Article

Does Enrichment Improve Reptile Welfare? Leopard geckos (Eublepharis macularius) respond to five types of environmental enrichment

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Abstract

Animal welfare is a high priority for pet owners and accredited zoos and aquariums. Current approaches to measuring welfare focus on identifying consensus among behavioral and physiological indicators of positive and negative emotions. Environmental enrichment is a common strategy used to improve the welfare of captive animals. In enrichment programs, knowledge of an animal’s ecology and individual history are applied to modify the animal’s current environment and management to increase environmental complexity, make the environment more functional or natural, and increase behavioral opportunities. While enrichment techniques for primates and large mammals are well-studied, reptile enrichment has received little attention to date despite a few promising studies. In this study, we monitored the responses of 16 leopard geckos to five types of enrichment (Thermal, Feeding, Olfactory, Object, and Visual) using a repeated-measures design. We measured both specific behaviors we expected to change in response to each enrichment type and four behavioral indicators of welfare: exploratory behavior, species-specific behaviors (behavioral thermoregulation and hunting), behavioral diversity, and abnormal repetitive behaviors. We found geckos interacted with all five types of enrichment at above-chance levels (i.e., no 95% CIs for engagement time overlapped with 0 sec). Geckos spent more time interacting with Thermal and Feeding enrichment than the other types (F(4,60) = 49.84, p < 0.001). Thermal, Feeding, Olfactory, and Object enrichments (but not Visual enrichment) changed specific relevant behaviors (e.g., Thermal enrichment altered thermoregulatory behaviors, Wilk’s lambda = 0.25, F(3,13) = 13.39, p < 0.001) and improved behavioral indicators of welfare (e.g., behavioral diversity, Wilks’ lambda = 0.30, F(12,178) = 12.31, p < 0.001). These results suggest that geckos respond to environmental enrichment, that their responses are predictable based on their ecology, and that environmental enrichment improves gecko welfare. As in mammals and birds, enrichments that address behavioral needs (here: thermoregulation and feeding) appear more effective than enrichments that simply provide novel stimuli to increase exploration. The extent to which our results can be generalized to other reptile species awaits further study, but we suggest that enrichment should be more widely used to improve reptile welfare.

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... There has been recent interest in using behavioural diversity measures, calculated from behavioural data, to provide an objective insight into the welfare of both individual and groups of animals by determining how much variation is shown in their behavioural repertoire [31][32][33][34][35]. Greater behavioural diversity is generally accepted as a positive indicator of welfare [31,34,35]. ...
... H Duration and H Rate [33] were calculated using Excel (Microsoft Corporation, 2021), where p i is the duration or frequency, respectively, of ith behaviour. A higher H value represents greater behavioural diversity [41]. ...
... To date, the most common method of assessing the behavioural impacts of enrichment items or enclosure changes in reptiles has been ethogram use, to assist in recording changes in behaviour and to create an activity budget [21][22][23]26,33]. Additionally, there are no studies assessing the welfare implications of reduced space for tortoises and, conversely, the welfare improvements to be gained by increasing space for tortoises. ...
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Reptile behaviour and welfare are understudied in comparison with mammals. In this study, behavioural data on three species (Astrochelys radiata, Stigmochelys pardalis, Aldabrachelys gigantea) of tortoises were recorded before and after an environmental change which was anticipated to be positive in nature. The environmental changes differed for each population, but included a substantial increase in enclosure size, the addition of substrate material, and a change in handling procedure. A tortoise-specific ethogram was created to standardise data collection. Focal behaviour sampling was used to collect behavioural data. Changes in the duration of performance of co-occupant interaction and object interaction in the leopard (Stigmochelys pardalis) and Aldabra (Aldabrachelys gigantea) tortoises were observed following the environmental changes. The Shannon–Weiner diversity index did not yield a significant increase after the changes but had a numerical increase which was relatively greater for the leopard tortoise group, which had experienced the greatest environmental change. The leopard tortoises also demonstrated changes in a greater number of behaviours compared to the other species, and this was sustained over the study period. However, this included a behaviour indicative of negative affect: aggression. Whilst we are unable to conclude that welfare was improved by the management changes, there are suggestions that behavioural diversity increased, and some promotion of positive social behaviours occurred.
... is an abnormal behaviour exhibited by lizards in captivity, including P. liolepis (e.g., Gómez et al., 1993), and has been previously used as an indicator of poor welfare in reptiles (Bashaw, Gibson, Schowe, & Kucher, 2016;Case et al., 2005;Manrod & Hartdegen, 2008;Warwick, 1990). Every day, after lights went on (8:00 hr), one observer (C.L.) recorded the occurrence of the afore-mentioned behaviours using scan sampling (every 15 min between 8:00 and 11:00 hr) and an instantaneous recording rule. ...
... To the best of our knowledge, there is only one previous paper addressing olfactory environmental enrichment in Euplepharis macularius (Bashaw et al., 2016). In this study, chemosensory enrichment consisted of presenting animals with one of two scented blocks (either mint or snake scent), which resulted in a significant increase in the time devoted to exploration and interaction with objects (Bashaw et al., 2016). ...
... To the best of our knowledge, there is only one previous paper addressing olfactory environmental enrichment in Euplepharis macularius (Bashaw et al., 2016). In this study, chemosensory enrichment consisted of presenting animals with one of two scented blocks (either mint or snake scent), which resulted in a significant increase in the time devoted to exploration and interaction with objects (Bashaw et al., 2016). However, the authors detected equivalent results for chemosensory and object enrichment, both consisting in the introduction of large items, but they were unable to distinguish the separate effect of each type of enrichment. ...
... There has been recent interest in using behavioural diversity measures, calculated from behavioural data, to provide an objective insight into the welfare of an individual, or group, of animals by determining how much variation is shown in their behavioural repertoire [31][32][33][34][35]. Greater behavioural diversity is generally accepted as a positive indicator of welfare [31,34,35]. ...
... Shannon Wiener's Diversity Index was used to calculate behavioural diversity before and after the environmental change. The formula for Shannon-Weiner's diversity index is [32]: H = -∑(pi*ln(pi)) HDuration and HRate [33] were calculated using Excel (Microsoft Corporation, 2021), where pi is the duration or frequency, respectively, of ith behaviour. A higher H value represents greater behavioural diversity. ...
... To date the most common method of assessing the behavioural impacts of enrichment items or enclosure changes in reptiles has been ethogram use, to assist in recording changes in behaviour and to create an activity budget [21][22][23]26,33]. Additionally, there are no studies assessing the welfare implications of reduced space for tortoises, and conversely the welfare improvements to be gained by increasing space for tortoises. ...
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Reptile behaviour and welfare are understudied in comparison with mammals. In this study, behavioural data on three species of tortoises were recorded before and after an environmental change which was anticipated to be positive in nature. The environmental changes differed for each population, but included a substantial increase in enclosure size, the addition of substrate material , and a change in handling procedure. A tortoise-specific ethogram was created to standardise data collection. Focal behaviour sampling was used to collect behavioural data. Changes in the duration of performance of co-occupant interaction and object interaction in the leopard (Stigmo-chelys pardalis) and Aldabra (Aldabrachelys gigantea) tortoises were observed following the environmental changes. The Shannon-Weiner's diversity index did not yield a significant increase after the changes but had a numerical increase which was relatively greater for the leopard tortoise group, which had experienced the greatest environmental change. The leopard tortoises also demonstrated changes in a greater number of behaviours compared to the other species, and this was sustained over the study period. However, this included a behaviour indicative of negative affect; aggression. Whilst we are unable to conclude that welfare was improved by the management changes, there are suggestions that behavioural diversity increased, and some promotion of positive social behaviours occurred.
... Furnishings must reflect the habitat and behavioral needs of animals, for example in respect of: terrestrial, burrowing, subterranean, arboreal, climbing, postural-positional, semiaquatic, aquatic characteristics (114). Accordingly, plant life (real or simulated), terrestrial mounds, deep substrates, rocks, as appropriate for the species should be provided in all environments (81,115). Bare and under-stimulating environments should not be utilized (44,116,117). ...
... Derived from reviewed literature (1,8,44,57,79,81,115,116). Cause/problem keys: 1 Overly restrictive/incorrect environment/inability to hide/retreat. 2 Co-occupant aggression/harassment. ...
... Biting/cannibalism 1,9,12 Derived from reviewed literature (1,8,44,57,79,81,115,116). Cause/problem keys: 1 Overly restrictive/incorrect environment/inability to hide/retreat. 2 Co-occupant aggression/harassment. ...
Article
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Various establishments exist in which animals are held for a variety of reasons. Historically, the management and inspection of animals in commerce and in private keeping have involved a considerable degree of arbitrary evaluation based on the personal experience of the vendor, keeper, advisor, or inspector. Accordingly, relevant protocols and standards are subject to considerable variation. Relatedly, diversity of traded and privately kept species generates significant challenges for those responsible for facility management and inspection alike. Animal welfare and public health and safety are constant and major concerns that require objective methodologies to monitor and control. This report focuses on establishments concerned with the boarding, breeding, storage, vending or handover of animals intended for human “companions” or “pets”, and aims to provide universal objective information for essential husbandry, inspection protocols and an allied inspection assessment tool for scoring establishments.
... One potential reason stereotypic behavior was not impacted was due to overall low levels observed throughout the study. Similar results were also seen in a study examining enrichment with leopard geckos with stereotypic behavior not being impacted but was performed at a low rate [38]. Similar findings were also observed in a study examining enrichment in wombats with no impact on stereotypic behavior, but the authors attributed it to not providing the correct type of enrichment [39]. ...
... In total, across 28 studies, there was a reported increase in behavioral diversity (decrease for lack of enrichment) for 78.6% of the studies, with the remaining 21.4% reporting no significant difference. Species that experienced an increase in behavioral diversity following enrichment or an enhanced habitat included big cats [27,45,46], leopard geckos [38], parakeets [33], capuchins [40], African cichlid males [47], pigs [21,[48][49][50], wombats [39], red foxes [51], bottlenose dolphins [52], ghost bats [53], bears (spectacled [30], Andean, sloth, brown, and black [54]), rats [55], African elephants [32], small felids [26], hognose snakes [56], giant pandas [28,29], and chimpanzees [31]. Species where enrichment or improved habitat was not found to significantly change behavioral diversity include armadillos, bush babies, and two toed sloths [57], wolves [58], African elephants [59], zebra fish and checker barbs [60], and lions [41]. ...
Article
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Modern day zoos and aquariums continuously assess the welfare of their animals and use evidence to make informed management decisions. Historically, many of the indicators of animal welfare used to assess the collection are negative indicators of welfare, such as stereotypic behavior. However, a lack of negative indicators of animal welfare does not demonstrate that an individual animal is thriving. There is a need for validated measures of positive animal welfare and there is a growing body of evidence that supports the use of behavioral diversity as a positive indicator of welfare. This includes an inverse relationship with stereotypic behavior as well as fecal glucocorticoid metabolites and is typically higher in situations thought to promote positive welfare. This review article highlights previous research on behavioral diversity as a potential positive indicator of welfare. Details are provided on how to calculate behavioral diversity and how to use it when evaluating animal welfare. Finally, the review will indicate how behavioral diversity can be used to inform an evidence-based management approach to animal care and welfare.
... Behavioral diversity is becoming more common as a measure of welfare in a variety of species. Bashaw et al. (2016) evaluated behavioral diversity as a measure of welfare in a study of leopard geckos (Eublepharis macularius) and showed it increased in response to thermal, feeding and olfactory enrichment. The results of the present study are consistent with those of Bashaw et al. (2016), as the snakes exhibited greater behavioral diversity in the modified habitats, largely due to increases in exploration behaviors and locomotion. ...
... Bashaw et al. (2016) evaluated behavioral diversity as a measure of welfare in a study of leopard geckos (Eublepharis macularius) and showed it increased in response to thermal, feeding and olfactory enrichment. The results of the present study are consistent with those of Bashaw et al. (2016), as the snakes exhibited greater behavioral diversity in the modified habitats, largely due to increases in exploration behaviors and locomotion. Miller et al. (2016) showed that behavioral diversity was negatively correlated with fecal glucocorticoid metabolite concentrations in cheetahs (Acinonyx jubatus), suggesting higher levels of behavioral diversity corresponded with reduced activity of the adrenal system. ...
... A number of these studies have examined the behavioral responses to provision of enrichment, as a method assumed to improve animal welfare. The occurrence of abnormal repetitive behaviors, such as escape behaviors [23], increased locomotor exploration, [24][25][26], increased foraging behaviors [24][25][26], behavioral response to novelty [25], along with increased visibility and loose-coiling whilst resting in snakes [27], have all been proposed as useful methods to ascertain welfare. Other behaviors suggested as indicators of stress in reptiles include body inflation and hissing, aggression directed towards conspecifics and humans, and interaction with transparent boundaries [28][29][30]. ...
... A number of these studies have examined the behavioral responses to provision of enrichment, as a method assumed to improve animal welfare. The occurrence of abnormal repetitive behaviors, such as escape behaviors [23], increased locomotor exploration, [24][25][26], increased foraging behaviors [24][25][26], behavioral response to novelty [25], along with increased visibility and loose-coiling whilst resting in snakes [27], have all been proposed as useful methods to ascertain welfare. Other behaviors suggested as indicators of stress in reptiles include body inflation and hissing, aggression directed towards conspecifics and humans, and interaction with transparent boundaries [28][29][30]. ...
Article
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There is an increasing focus on evidence-based welfare assessment by animal care staff in zoos, along with a strong interest in animal welfare by the zoo-visiting public, to the extent that this can influence their choice of institutions to visit. Regulatory oversight of animal welfare standards continues to strengthen across many jurisdictions. Zoos are increasingly formalizing their practices with the development and refinement of evidence-based welfare assessment tools. There has been a drive for welfare assessment tools to comprise both resource-based and animal-based measures. However, animal-based indicators are not always well characterized, in terms of their nature and whether they infer a positive or negative affective state. This is especially so for reptiles, which are often considered behaviorally inexpressive and are under-researched. In this study, a Delphi consultation approach was used to gather expert opinion on the suitability of potential animal-based indicators of welfare for inclusion in a welfare assessment tool across four families of reptiles: Agamidae, Chelidae, Pythonidae, and Testudinidae. Two rounds of online surveys were conducted eliciting responses from a global group of professionals who work with reptiles. In the first survey, respondents were provided with an author-derived list of potential animal-based indicators for consideration of their validity and practicality as welfare indicators. The indicators were refined for the second survey including only those indicators that were considered valid or practical on the first survey (≥4 on a 5-point Likert scale), and that achieved ≥70% consensus amongst experts. In the second survey, respondents were asked to re-evaluate the reliability and practicality of the indicators and to rank them on these facets. Eight to ten assessment indicators for each family of reptiles were identified from Survey 2. These indicators were often health related, for example, presence of oculo-nasal discharge or wounds. However, some true behavioral indicators were identified, such as showing species-specific interest and alertness. These indicators should now be incorporated into taxon-tailored welfare assessment tools for trial and validation in captive reptile populations. This study provides a next step towards developing reptile-specific animal welfare assessment tools for these often-overlooked animals.
... Bashaw [124] highlights that an animal's welfare state is influenced by its perception of the environment in which it lives. This individual perception is, in turn, influenced by the animal's evolutionary history (as discussed above), temperament and previous experience. ...
... This individual perception is, in turn, influenced by the animal's evolutionary history (as discussed above), temperament and previous experience. As such, two individuals of the same species housed in the same environment and provided with the same husbandry will not necessarily perceive the environment in the same way and, as a result, may have very different welfare outcomes [124][125][126]. Over the past 20 years there has been an exponential increase in the number of studies published on animal temperament and its implications for animal welfare and management in captive institutions [127]. ...
Article
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Achieving and maintaining high standards of animal welfare is critical to the success of a modern zoo. Research has shown that an animal’s welfare is highly dependent on how various individual animal factors (e.g., species traits, genetics, temperament and previous experience) interact with environmental features (e.g., social grouping, enclosure design and sensory environment). One prominent feature of the zoo environment is the presence of visitors. Visitor contact can be unpredictable and intense, particularly in terms of auditory and visual interaction. Depending on an animal’s perception of this interaction, visitors can have either negative, neutral or positive impacts on zoo animal behaviour and welfare. This paper reviews the literature on the implications and potential opportunities of human-zoo animal interactions on animal behaviour and welfare, with the aim of stimulating interest, understanding and exploration of this important subject. The literature to date presents a mixed range of findings on the topic. It is possible this variation in the responses of zoo animals to visitors may be due to species-specific differences, the nature and intensity of the visitor interactions, enclosure design, and individual animal characteristics. Analysing these studies and better understanding animal preferences and motivations can provide insight into what animals find negatively and positively reinforcing in terms of visitor contact in a specific zoo setting. This understanding can then be applied to either safeguard welfare in cases where visitors can have a negative impact, or, conversely, it can be applied to highlight opportunities to encourage animal-visitor interaction in situations where animals experience positive emotions associated with visitor interaction.
... Novel object enrichment (Burghardt et al. 1996;Therrien et al. 2007;Mehrkham and Dorey, 2014;Bashaw et al. 2016) and structural enrichment (Case et al. 2005;Rose et al. 2014;Tetzlaff et al. 2018) reduced repetitive behaviours and increased levels of activity in turtles. Coloured object enrichment reduced the escape behaviour and increased the level of activity of a group of captive river cooters Pseudemys sp. and pond sliders Trachemys scripta before feeding, but there were differences in the direction of change in escape behaviour at individual level (Bannister et al. 2021), indicating that it is important to study the impact of any new enrichment not only at group level, but also on each individual concerned. ...
... Coloured object enrichment reduced the escape behaviour and increased the level of activity of a group of captive river cooters Pseudemys sp. and pond sliders Trachemys scripta before feeding, but there were differences in the direction of change in escape behaviour at individual level (Bannister et al. 2021), indicating that it is important to study the impact of any new enrichment not only at group level, but also on each individual concerned. Turtles have consistent behavioural types (Waters et al. 2017) and individual perception and preferences may strongly influence health and wellbeing (Bashaw et al. 2016). Bolder, more curious and explorative individuals may be more deprived and stressed in a limited space or with lack of novelty items, while shy, fearful ones may be more stressed by new challenges and need more places to hide (Richter and Hintze 2019). ...
Article
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Recent studies showed that freshwater turtles display inter-individual differences in various behavioural traits, which may influence their health and welfare in captivity due to differences in response to husbandry and enrichment strategies and in ability to cope with the limitations of the captive environment. This study investigated a possible correlation between individual level of escape behaviour under standard enrichment conditions and level of interest in coloured objects in a group of cooters Pseudemys sp. and sliders Trachemys scripta ssp. on display at a public aquarium. Interest in different colours, colour preference and individual differences in behavioural changes in the presence of the new enrichment were also studied. Turtles categorised as 'high' and 'moderate escape behaviour' (17-34% of behavioural budget) showed more interest in coloured objects and tended to display less escape behaviour in their presence, while turtles categorised as 'low escape behaviour' (<10% of behavioural budget) were less interested in coloured objects and tended to display more escape behaviour in their presence. Overall, there was more interest in yellow than in red, white or green objects, with more contacts with coloured objects before feeding and at the start of each observation period and a preference for yellow against red objects. The individual differences in behavioural changes in the presence of the new enrichment suggested that more studies into colour preference and response to novelty in turtles would be beneficial to ensure that no individuals are unduly stressed by new enrichments.
... Environmental enrichment (referred to as enrichment hereafter) is used to improve the health and welfare of species managed ex situ, one desired outcome of which is the broadening of an individual's behavioural repertoire [1]. Reptile enrichment methods have historically been based on the anecdotal evidence of caregivers, often drawn from experience with a limited group of individuals [2,3]. ...
... As such, there is limited information describing the impacts (positive and negative) of these methods [4][5][6][7], including the extent to which different types of enrichment affect behaviour, and the longevity of these effects [8][9][10]. However responsible, modern collections require robust, quantitative evidence on which to base husbandry decisions; despite an increasing focus on herptile enrichment, this is still lacking for reptiles [1,3,6]. ...
Article
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Environmental enrichment has been shown to enhance the behavioural repertoire and reduce the occurrence of abnormal behaviours, particularly in zoo-housed mammals. However, evidence of its effectiveness in reptiles is lacking. Previously, it was believed that reptiles lacked the cognitive sophistication to benefit from enrichment provision, but studies have demonstrated instances of improved longevity, physical condition and problem-solving behaviour as a result of enhancing husbandry routines. In this study, we evaluate the effectiveness of food- and scent-based enrichment for three varanid species (Komodo dragon, emerald tree monitor lizard and crocodile monitor). Scent piles, scent trails and hanging feeders resulted in a significant increase in exploratory behaviour, with engagement diminishing 330 min post provision. The provision of food- versus scent-based enrichment did not result in differences in enrichment engagement across the three species, suggesting that scent is just as effective in increasing natural behaviours. Enhancing the environment in which zoo animals reside is important for their health and wellbeing and also provides visitors with the opportunity to observe naturalistic behaviours. For little known and understudied species such as varanids, evidence of successful (and even unsuccessful) husbandry and management practice is vital for advancing best practice in the zoo industry.
... Approaches similar to Case [15] and Tetzlaff [16], who used an evidence based approach comparing minimalistic with naturalistic care, and documented increased stress in Terrapene carolina (Eastern Box turtles) maintained in simple versus complex conditions, help support one approach over another. Regarding behavioral enrichment, reptiles time and time again have been shown in scientific studies to respond to complex captive environments [11,[15][16][17], complex thermal repetoires [11,18,19], and complex diets [11,18] in ways that decrease stress and demonstrate choice. Evidence based husbandry has become a favorable herpetocultural approach [11,12,14], specifically to those who hope to avoid folklore husbandry practices [11,14]. ...
... Approaches similar to Case [15] and Tetzlaff [16], who used an evidence based approach comparing minimalistic with naturalistic care, and documented increased stress in Terrapene carolina (Eastern Box turtles) maintained in simple versus complex conditions, help support one approach over another. Regarding behavioral enrichment, reptiles time and time again have been shown in scientific studies to respond to complex captive environments [11,[15][16][17], complex thermal repetoires [11,18,19], and complex diets [11,18] in ways that decrease stress and demonstrate choice. Evidence based husbandry has become a favorable herpetocultural approach [11,12,14], specifically to those who hope to avoid folklore husbandry practices [11,14]. ...
Article
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Herpetocultural practices are based on norms driven by economy of space and time for keepers, with little scientific inference backing their practice. In recent years, a subset of herpetoculturalists have promoted evidence-based husbandry that relies on science and experimental design to generate husbandry practice. A theoretical framework and protocol are proposed herein that enables any individual who has access to the internet the ability to use various outlets of natural history information (scientific literature databases, social media sources, and weather websites) and previously published husbandry reports as evidence to drive the creation of novel herpetocultural practice. A case study is provided which compares readily available information on the care of Hydrodynastes gigas (false water cobra), such as online care sheets for the species, with the proposed evidence based herpetocultural protocol founded on natural history information and published care and captive breeding reports. Results were assessed for protocol efficacy and determined that the natural history informed evidence-based approach increased animal welfare and generated new information specific to the natural history of H. gigas.
... However, these are time-intensive and difficult to apply to the wide variety of species held in zoos, let alone the multitude of extant reptiles [23]. Bashaw et al. (2016) used preference testing to examine the response of leopard geckos (Eublepharis mascularius) to five types of enrichment. The geckos responded predominantly to thermal and feeding enrichment, perhaps because these address the behavioral needs of this species [24]. ...
... Bashaw et al. (2016) used preference testing to examine the response of leopard geckos (Eublepharis mascularius) to five types of enrichment. The geckos responded predominantly to thermal and feeding enrichment, perhaps because these address the behavioral needs of this species [24]. This agrees with the idea that effective enrichment strategies should be based on a motivation, rather than being designed to 'distract' or 'entertain' the animal, as a random novelty might achieve [25]. ...
Article
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Reptiles are held at wildlife parks and zoos for display and conservation breeding programs and are increasingly being kept as pets. Reliable indicators of welfare for reptiles need to be identified. Current guidelines for the captive management of reptiles utilize resource-based, rather than animal-based indicators; the latter being a more direct reflection of affective state. In this paper we review the literature on welfare assessment methods in reptiles with a focus on animal-based measures. We conclude that, whilst a number of physiological and behavioral indicators of welfare have been applied in reptiles, there is need for further validation of these methods across the diversity of species within the Class. Methods of positive welfare state assessment are comparatively understudied and need elucidation. Finally, we examine some widely-used welfare assessment tools in mammals and explore the application of the Welfare Quality® Protocol to the endangered pygmy blue-tongue skink, Tiliqua adelaidensis. We propose that this framework can form the basis for the development of taxon-specific tools with consideration of species-specific biology.
... Despite the attention bias, this is a developing field (Figure 1), and the studies that have been published in peer-reviewed journals support the notion that reptiles benefit from enrichment [21,[26][27][28][29][30][31] and that it is in fact essential [32]. Evidence for enrichment as a beneficial practice with reptiles is documented through an increase in natural behaviors and relaxed postures under structural enriched environments [33,34]. ...
... Similarly, the use of fishscented enrichment cups resulted in a reduction in escape behaviors of aquarium-housed, freshwater turtles (Trachemys scripta and Pseudemys concinna), although there was an increase in aggression, which demonstrates the need to assess the efficacy of any new techniques before implementation [35]. When offered multiple forms of enrichment, leopard geckos (Eublepharis macularius) interacted with all forms and, in particular, to a feeding puzzle and to structural enrichment placed under a heat source [31]. The alternative forms, sensory (mirror and olfactory) and novel object enrichment, elicited less engagement; however, this highlights that the enrichment should be species-specific and biologically or ecologically relevant. ...
Article
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Enrichment has become a key aspect of captive husbandry practices as a means of improving animal welfare by increasing environmental stimuli. However, the enrichment methods that are most effective varies both between and within species, and thus evaluation underpins successful enrichment programs. Enrichment methods are typically based upon previously reported successes and those primarily with mammals, with one of the main goals of enrichment research being to facilitate predictions about which methods may be most effective for a particular species. Yet, despite growing evidence that enrichment is beneficial for reptiles, there is limited research on enrichment for Varanidae, a group of lizards known as monitor lizards. As a result, it can be difficult for keepers to implement effective enrichment programs as time is a large limiting factor. In order for appropriate and novel enrichment methods to be created, it is necessary to understand a species’ natural ecology, abilities, and how they perceive the world around them. This is more difficult for non-mammalian species as the human-centered lens can be a hinderance, and thus reptile enrichment research is slow and lagging behind that of higher vertebrates. This review discusses the physiological, cognitive, and behavioral abilities of Varanidae to suggest enrichment methods that may be most effective.
... The latter is a very important behavior in reptiles and the time they spend thermoregulating is strongly related to active behaviors: foraging, reproduction and feeding (Rocha, Vrcibradic, Kiefer, de Menezes and da Costa Siqueira, 2009). Enrichment produces changes in the thermal behavior of some reptiles (Bashaw, Gibson, Schowe and Kucher, 2016). In this case, a decrease in this activity is observed during enrichment, both when compared with R1, and R2WE. ...
... Based on the application of enrichment in mammals, an increase in exploratory activity and a decrease in resting time or sedentary lifestyle would be expected (Refuge in this study). In Salvator, only a decrease in the time spent in the refuge was observed (Figure 2), unlike what occurs in Eublepharis macularius, in which enrichment did not affect this behavior (Bashaw et al., 2016). "Exploratory activity" did not change significantly with enrichment, which could be explained by two possibilities: 1) the quality of the sites in terms of exploration opportunities is very similar; they are large open-air sites with water and shelter available; and, 2) that the changes in exploratory behavior in the enrichment enclosure have been masked in the "Other" category ( Figure 2) where behaviors such as digging to find food and scratching logs that imply some types of exploratory behavior were recorded (sniff, sniffing while moving). ...
Article
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Environmental enrichment seeks to improve the quality of care for animals in captivity through the constant generation of new sources of stimuli to simulate a complexand changing environment. Salvator merianae is a species of large lizard whose native distribution covers the subtropical and humid zones of southeastern South America. The study was carried out in the Experimental Lizard Hatchery belonging to the Facultad de Agronomía y Zootecnia from Universidad Nacional de Tucumán, UNT for its initials in Spanish. Two pens were used, a control group R1 (Enclosure 1) and an experimental group R2 (Enclosure 2), where data were taken ithout enrichment (R2 W/O-E) and with enrichment (R2 WE). An ethogram was used to record the different behaviors that were then grouped into eight categories to evaluate how animals spend their time. Behaviors were recorded on video, the applied technique was the focal animal sampling with instantaneous recording, the extracted data were ex- ported into individual spreadsheets. The Landau index was calculated to determine the existence of hierarchies. The data suggest that the modification of the enclosure conditions has the capacity to alter the behavioral profiles. Only a few behavioral categories showed significant differences. No significant differences were found, in the frequency of the behavioral categories, between males and females. There was a decrease in the frequency of reproductive behavior in males in R2. There was a non-linear hierarchy among the individuals. A ecrease in the chases was observed among individuals in R2.
... Zoo animal welfare is often linked to the behavior of zoo animals-and quite rightly so. The diversity and duration of behaviors demonstrated by a particular animal are useful in indicating its psychological state [45,46] and may also have implications for conservation success [47]. Of course, behavior alone does not always give us a comprehensive insight into an animal's welfare state-for example, an animal may be behaving normally but may be physically unhealthy and thus its welfare may be compromised, but despite this potential limitation, an animal's behavior often gives us important information about how that animal feels. ...
... Understanding animal behavior is essential to the early detection of zoo animal welfare problems. It is recognized that a variety of abnormal repetitive behaviors (ARBs) comprising but not limited to stereotypic ritualistic behavior (pacing, head-tossing), self-directed behaviors (feather-plucking, over-grooming), or externally directed behaviors (conspecific mutilation, barrel-pouncing in polar bears), are common in many species held in zoos, e.g., canids, bears, elephants, primates, ruminants [9], birds [50,51] and even occur in less charismatic species such as fish and reptiles [46,[52][53][54]. Often these ARBs may be dismissed merely as 'behavior problems' when in actuality their origin from repeated attempts to cope, behavioral frustration, or psychopathology [55] may actually indicate psychological distress and thus poor welfare. ...
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Simple Summary This paper outlines some of the barriers to implementing improved zoo animal welfare in practice, and proposes a new strategy for the development of behavioral husbandry routines focused on the management and mitigation of abnormal repetitive behaviors. Focusing on enhancing zoo animal welfare by integrating aspects of ecology, ethology and clinical animal behavior into a practical and comprehensive approach to behavior-based husbandry. Abstract The field of zoo animal welfare science has developed significantly over recent years. However despite this progress in terms of scientific research, globally, zoo animals still face many welfare challenges. Recently, animal welfare frameworks such as the five domains or five needs have been developed and suggested to improve the welfare of zoo animals, but without practical guidance, such tools may remain abstract from the daily experience of zoo animals. Similarly specific practical strategies such as those for enrichment development exist, but their lack of holistic integration with other aspects of animal husbandry and behavioral medicine means that overall, good zoo animal welfare may still be lacking. This paper outlines some of the barriers to implementing improved zoo animal welfare in practice, and proposes a new strategy for the development of behavioral husbandry routines focused on the management and mitigation of abnormal repetitive behaviors. Focusing on enhancing zoo animal welfare by integrating aspects of ecology, ethology and clinical animal behavior into a practical and comprehensive approach to behavior-based husbandry.
... The effectiveness of new enrichments is usually assessed based on frequency of use and behavioral changes, with decreases expected in stress indicators (Bishop, Hosey & Plowman, 2013). Individual perception may vary (Bashaw, Gibson, Schowe & Kucher, 2016) and more curious and explorative individuals may suffer more in a limited unstimulating space, while fearful ones may need more hiding places or be stressed by new objects (Richter & Hintze, 2019). ...
Article
The effect of environmental enrichment on the behavior and welfare in captivity of reptiles and of freshwater turtles in particular, which are popular aquarium and pet species, is very little studied compared to other taxa. We carried out a small scale case‐study on the effect of colored object enrichment, with and without fish scent, on the behavior of a group of 15 cooters (Pseudemys sp.) and sliders (Trachemys scripta ssp.) on display at a public aquarium. The new enrichment aimed to reduce the escape behavior (interaction with transparent boundaries) and increase exploration and random swimming. We used simultaneous recording of behavior at whole group level and for focal individually‐marked turtles. The escape behavior decreased on days with new enrichment before feeding at whole group level and for the focal turtles overall, in spite of the relatively low interest in the colored objects. Fish‐scented objects attracted significantly more interest. Random swimming, enrichment focus, aggression and submission increased significantly, and basking decreased significantly at whole group level before feeding, with smaller differences after feeding. There were large differences between individual turtles with respect to activity budgets and changes in behavior on days with new enrichment, with both increases and decreases seen in escape behavior, aggression, and levels of activity. Our outcomes suggested that introducing new colored objects with food scent may be beneficial for reducing escape behavior in captive freshwater turtles. However, careful monitoring of effects at individual level and much larger scale investigations, including postenrichment periods, are needed. Research Highlights • The presence of colored objects reduced the escape behavior of freshwater turtles, mainly before feeding. • There was more interest when the new objects were fish‐scented. • There were differences in behavior and response to enrichment at individual level.
... Applied research should be used to inform these policy documents. There is a growing body of published work on applied animal welfare science in the zoo sector which explores the welfare consequences of various factors such as enrichment provision [14][15][16], enclosure design [17][18][19], social groupings [20], and human impacts [21][22][23][24]. This type of research is valuable in informing housing and husbandry standards for zoos, and clearly further study is needed to address the wide taxonomic spread of species housed in these settings. ...
Article
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There is a growing interest and need for zoos to develop and implement welfare assessment tools that are practical to use and provide meaningful results that can inform management decisions. This paper presents a process that was developed to support this type of evidence-based management in zoo animal welfare. The process is configured to facilitate institutional risk assessment, using an adapted version of the Five Domains Model for animal welfare assessment. It is designed to systematically analyse information gathered from zoo personnel in order to highlight areas of welfare risk, as well as areas that are performing well and areas requiring further investigation. A trial was conducted on three zoos over three years. Results of the trial suggest the process developed is practical and effective in identifying areas of welfare risk in a wide range of species in a zoo setting. It represents a further step towards achieving high-level animal welfare in zoos by integrating animal welfare as an institutional priority. The more zoos that employ such strategies, the greater the ability of the sector to advance the welfare of the animals in their care.
... les insectívoros en vida libre tienen una dieta basada en una gran variedad de presas dependiendo de la temporada del año difiriendo en la diversidad de insectos y la disponibilidad de éstos (Therry et. al., 1994;Aowphol et. al., 2006;Rouag et. al., 2007;Eyte-Manrique y Ramírez Bautista, 2010;Hardy, 2010;Maneyro y Panzera, 2014;Semmar y Roux, 2014;Gibson, et. al., 2016) y, según Álvarez del Toro y Smith en 1963, observaron que los dragoncitos de labios rojos se alimentaban de crustáceos, insectos, arácnidos y pequeños lagartos eslizones, refiriendo a que la dieta de éstos individuos no era monotípica, lo cual pudo ser una razón por la cual los dragoncitos en éste estudio dejaron de alimentarse, ya que ...
Thesis
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El dragoncito de labios rojos (Abronia lythrochila), es una especie de reptil arborícola, endémico de México, se ubica dentro del comercio internacional como animal de compañía no convencional, encontrándose actualmente en peligro de extinción, por lo que es indispensable conocer las necesidades nutricionales de la especie y así lograr un mayor éxito en su conservación y mantenimiento en condiciones de cautiverio. El objetivo de este trabajo fue determinar el consumo voluntario y la absorción aparente de los minerales Ca, P, Mg, Na, K, Mn, Fe, Cu y Zn, al ofrecer como dieta dos diferentes presas. Se utilizaron un total de 12 individuos agrupados en dos tratamientos; T1 (n=6) alimentados con tenebrios (Tenebrio molitor) y T2 (n=6) alimentados con grillo doméstico (Acheta domestica). El trabajo se llevó a cabo en la estación Biológica del Parque Educativo San José (San Cristóbal de las Casas, Chiapas), donde los animales fueron alojados en terrarios individuales, bajo condiciones propias de la región y en los Laboratorios de Bromatología y Toxicología de la FMVZ-UNAM. No se encontró diferencia significativa entre los tratamientos en el consumo voluntario y absorción aparente de los minerales, sin embargo se observó una reducción del consumo voluntario en ambos tratamientos a través del tiempo (siendo más evidente en el T2), resultando a su vez en una menor absorción aparente de los elementos minerales evaluados, lo cual promovió que en algunos casos tanto en la absorción aparente de los elementos minerales (Na) y el consumo mineral (Ca, Mg, K y Na), se obtuviera una diferencia significativa a través del tiempo. En el caso del Zn y el Cu, se observó una interacción entre tiempo y tratamiento en el consumo de los minerales. Se concluyó que las dietas monotípicas (de un solo ingrediente), no proporcionan las cantidades adecuadas de nutrientes, además de que pueden promover la disminución del consumo de alimento, e incluso anorexia, debido a que estas se vuelven monótonas para el animal.
... One purpose of enrichment is to increase naturalistic behaviors of exhibited animals through the introduction of stimuli and/or changes in feeding opportunities. Included among these have been the use of particular food presentations with bears (Andrews & Ha, 2014;Carlstead, Seidensticker, & Baldwin, 1991;Law, Boyle, Johnston & MacDonald, 1990), and with felids (Lyons, Young, & Deag, 1997;Shepherdson, Carlstead, Mellen, & Seidensticker, 1993), effects of acoustic "prey" on African leopards (Markowitz, Aday, & Gavazzi, 1995), inedible, manipulable objects given to zoo and aquarium animals (Altman, 1999;Bashaw, Gibson, Schowe, & Kucher, 2016;Clark, Davies, Madigan, Warner, & Kuczaj, 2013), enclosure manipulations, including choice between enclosures (Carlstead, Brown, & Seidensticker, 1993;Sherwin, Lewis, & Perry, 1999), and access to conspecifics or stimuli associated with conspecifics (Bourgeois & Brent, 2005;Mills & Riezebos, 2005). ...
Article
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The modern zoo has brought about two major advances in the behavioral welfare of their exhibited animals: (a) The use of environmental enrichment to promote naturalistic behaviors and (b) the use of training to improve voluntary husbandry care. Whereas training itself has been talked about as an effective enrichment strategy, little has been done to combine training procedures with enrichment. Typically, enrichment is treated as a trial and error process, where potential enrichment items or procedures are cycled through until successful enrichment is found. The use of shaping or other training techniques has seldom been documented to increase engagement with possible enrichment items or procedures. The following study examined the possibility of combining training and enrichment to produce continued interactions with enrichment devices. Two species of penguin, Magellanic and southern rockhopper penguins, were studied. Two measures were taken: Time spent swimming and contact with enrichment devices. The enrichment devices could be manipulated by placing fish within and hanging out of each device. During baseline sessions, no hits to either device were observed. During training sessions, several hits were recorded when fish were in the devices and overall swimming time increased during these conditions. When baseline was reintroduced without fish in the devices, contact with the enrichment devices rapidly declined and swimming time for the rockhopper penguins decreased. When the devices were reintroduced with fish but without training, the greatest number of enrichment device contacts and the highest percentage of time spent swimming were observed for the rockhopper penguins.
... For example, animals can be trained to press a lever that has been associated with different people or animals to indicate who they want to spend time with (Adams and MacDonald 2018). This technique can also be used for allowing the animal to choose a reinforcer (see Figure B4.2) (Fernandez et al. 2004;Gaalema et al. 2011), enrichment items (Bashaw et al. 2016;Fay and Miller 2015;Dorey 2014, 2015), or even between enrichment and training . This box will give a short overview of marine mammal training examples and opportunities. ...
... To combat morphological and behavioral deficiencies, some head- starting programs have incorporated environmental enrichment tech- niques (see Bashaw et al., 2016;Biggins et al., 1998;Salvanes et al., 2013). Environmental enrichment aims to mimic nature by introducing captive animals to live prey, incorporating more natural refugia, structural complexity, and microhabitat characteristics, and training them to adopt appropriate survival skills prior to release (Biggins et al., 1998;Ward and Hilwig, 2004;Alberts, 2007). ...
... Los estudios sobre contra-freeloading han demostrado que muchos animales en determinadas circunstancias prefieren trabajar para un recurso como la comida, en lugar de tener un acceso fácil a él, y que la provisión de tareas de resolución de problemas puede resultar en estados afectivos menos negativos y comportamientos más normales (Wolfensohn et al., 2018). Existe un cuerpo creciente de evidencia científica que explora los beneficios del enriquecimiento ambiental para el bienestar animal, incluso en taxones poco explorados como los reptiles (Bashaw et al., 2016;Wagman et al., 2018). ...
Research
Mantener un alto nivel de bienestar animal es esencial en los zoológicos por razones éticas y legislativas. Surge, entonces, la necesidad de contar con herramientas de evaluación para monitorear y mejorar el bienestar de los animales alojados en estas instituciones. Sin embargo, la mayoría de los protocolos de que se dispone actualmente fueron desarrollados para animales de granja o de laboratorio e insumen mucho tiempo para su aplicación. Por ello urge disponer de herramientas de evaluación del bienestar animal válidas, confiables, y aplicables que puedan incorporarse en los programas diarios de manejo y reproducción en los zoológicos. El enfoque más común para la evaluación del BA consiste en cuantificar los recursos disponibles, los parámetros ambientales y las buenas prácticas. Empero, los actuales avances científicos remarcan la necesidad de incorporar indicadores basados en el animal o directos, que consideren la percepción y experiencia del individuo, incluyendo su estado afectivo. El objetivo de este trabajo fue desarrollar un protocolo para la evaluación del bienestar animal, que pudiera aplicarse en diferentes especies de fauna silvestre (mamíferos, aves y reptiles) en cautiverio, integrando indicadores basados en el animal (directos), en el ambiente y en los recursos (indirectos). En la primera etapa se llevó a cabo una revisión sistemática de artículos científicos consultando diferentes buscadores, repositorios y bases de datos académicas, con fecha desde 2008 a la actualidad, en inglés y español. Se obtuvieron 34 resultados de los cuales, luego de su lectura, se seleccionaron 24. A partir de estos documentos se escogieron 40 indicadores, los cuales fueron divididos en 11 criterios y 5 aspectos. Para continuar este trabajo, los indicadores seleccionados se someterán a la determinación de confiabilidad (concordancia inter e intra- observador) y practicidad, para finalmente ponerlo a prueba en distintas instituciones y con diversas especies de mamíferos, aves y reptiles. El uso de protocolos de este tipo podría incrementar las oportunidades para mejorar la calidad de vida de los animales alojados en zoológicos, aumentar su valor intrínseco de conservación y optimizar los recursos humanos y económicos con que cuentan estas instituciones.
... 58 However, green iguanas without climbing opportunities have elevated corticosterone metabolite levels. 59 Furthermore, Nile soft-shelled turtles 60 and sea turtles 61,62 showed interest in playing with an object, whereas this was not the case for leopard geckos. Especially large reptile species, such as monitors, tortoises, and crocodilians, can learn and solve problems. ...
Chapter
The provision of a good light source is important for reptiles. For instance, ultraviolet light is used in social interactions and used for vitamin D synthesis. With respect to housing, most reptilians are best kept pairwise or individually. Environmental enrichment can be effective but depends on the form and the species to which it is applied. Temperature gradients around preferred body temperatures allow accurate thermoregulation, which is essential for reptiles. Natural distributions indicate suitable ambient temperatures, but microclimatic conditions are at least as important. Because the nutrient requirements of reptiles are largely unknown, facilitating self-selection from various dietary items is preferable.
... Providing environmental enrichment is widely considered one of the most effective strategies for promoting psychological well-being (Swaisgood and Shepherdson 2005;de Azevedo et al. 2007;Makecha and Highfill 2018); therefore, this emphasis may not be surprising. The taxonomic focus of enrichment studies has historically been biased toward large, charismatic species (Swaisgood and Shepherdson 2005) although recent work has begun to expand welfare evaluations of environmental enrichment to lesser studied taxa, such as reptiles and amphibians (e.g., Burghardt 2013; Bashaw et al. 2016). It seems likely that a focus on enrichment will remain a cornerstone of zoo and aquarium research moving forward as technology continues to develop and expand the scope of potential enrichment approaches, including for example tablet computers for apes or automated feeders coupled with motion detection for giraffes (e.g., Kim-McCormack et al. 2016;Krebs and Watters 2016; see also Clay et al. 2011;Clark 2017). ...
Article
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Research into the conditions that promote good animal welfare is essential to equip zoos and aquariums with the knowledge to create environments in which animals thrive. In order to collate the empirical information that is available regarding animal welfare in zoos and aquariums with regard to topics, methods and species, a systematic literature review was conducted of the primary peer-reviewed journals publishing zoo-based and welfare-based research. Journals included Animal Welfare, Animals, Applied Animal Behaviour Science, International Zoo Yearbook, Journal of Applied Animal Welfare Science, Journal of Zoo and Aquarium Research, and Zoo Biology. The literature review spanned 2008–2017 and revealed that 7.6% (n=310) of reviewed publications (n=4,096) in these journals were zoo- or aquarium-based and animal-welfare focused. The main topics studied included enrichment, social conditions and enclosure design, while understudied topics included the welfare of ambassador animals, and the welfare impacts of sound and light. Behaviour was by far the dominant welfare parameter used and the use of hormonal measures declined over this period. Taxonomic representation in these publications was notably skewed. Mammals were the focus of 75% of studies, and 82% of studies were vertebrate-focused (great apes being the dominant taxa). This study considers potential reasons for these patterns and highlights research areas for future emphasis that could serve to fill gaps in current knowledge regarding zoo and aquarium animal welfare, including more research into affective states that underlie an animal’s welfare status.
... Burghardt et al. (1996) studied enrichment use in Nile soft-shelled turtles (Trionyx triunguis) and found that they would often play with enrichment when it was provided, as long as they were kept in optimal conditions. Bashaw et al., (2016) conducted an environmental enrichment experiment with Leopard Geckos (Eublepharis macularis) that indicated that enrichment based on behavioural needs are more successful than novelty enrichments. Almli and Burghardt, (2006) conducted a study of enrichment in Elaphe ratsnakes. ...
Thesis
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To date, there has been relatively little research conducted pertaining to behaviour in Reptilia, particularly in the area of enrichment. This is especially true for crocodilians, which are somewhat neglected in the literature in favour of more charismatic animals such as birds and mammals. The primary aim of this study was to test three forms of environmental enrichment to see whether they could influence the behaviours of crocodilians at Paignton Zoo, England and whether individual differences or time would also be factors in these differences. Binary logistic modelling found that all three factors, enrichment (Wald Chi-Square=54.003, d.f.=3, p<0.001), individual (Wald Chi-Square=558.697, d.f.=5, p<0.001) and time class (Wald ChiSquare=119.177, d.f.=5, p<0.001), had a significant effect on the crocodilians use of the pools incorporated within their enclosures. All three enrichment types had significantly different effects from one another. Watermelon (x̄=1.528, S.E.=0.143) was the most effective at encouraging crocodiles to use the water portion of their enclosure, compared against the control condition (x̄=2.287, S.E.=0.149). The boomer ball containing meat (x̄=2.416) had no significant effect compared to the control, however cork bark (x̄=3.062, S.E.=0.178) had significantly reduced water use. A following binary logistic test revealed that enrichment (Wald ChiSquare=4.039, d.f.=3 p=0.257) had no effect on promoting locomotive activity in the crocodiles. The variety in effectiveness of enrichment reinforces the idea that objective testing is required to understand whether enrichments provided are having the effect intended, or whether they are instead having no, or the opposite effect, with a representative from all three scenarios being shown in this study. Further studies should also look to examine why certain enrichments are more effective than others to help identify potential future enrichment with the highest chance of success.
... Evaluations of reptile behavior and welfare, though increasing [64][65][66], are still infrequent, occurring at rates well below those of other taxa [28]. With such a strong need to evaluate the welfare of reptiles within zoological parks, one overarching question is where to begin? ...
Article
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Visitor presence has been shown to affect the behavior of animals in zoos. However, studies to date have not included a wide range of taxonomic groupings, and thus, the effect is poorly understood for many species. Here, we compared the behavior of Nile crocodiles (Crocodylus niloticus) in the presence and absence of visitors for the first time. Data were collected at Disney’s Animal Kingdom® over two months during normal operating conditions and during the same two months the following year when the park was closed due to the COVID-19 pandemic, totaling 158 observation hours. Significant differences in crocodile behavior were observed between park operating conditions; however, the direction of change varied by behavior and average differences were generally small. In addition, we found that time of day, temperature and month significantly affected behavior, often with greater magnitude than visitor presence. This highlights the importance of accounting for environmental variables when evaluating and interpreting the behavior, and ultimately welfare, of reptiles in zoos. Collectively, the data suggest the overall effect of visitors on crocodile behavior was small and neutral from a welfare perspective. This study highlights the importance of taxonomic diversity in studying the visitor effect.
... In the interest of following the logic, using measures of behavioral diversity as a proxy measure of animal welfare has increased in recent years [10,[78][79][80]. The most commonly used behavioral diversity index, the Shannon-Wiener Diversity index (H-index, [81,82]), is useful for quantifying whether an animal's time budget is heavily skewed towards a few behaviors (low H-index) or spread across multiple behavioral categories (high Hindex). ...
Article
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An emphasis on ensuring animal welfare is growing in zoo and aquarium associations around the globe. This has led to a focus on measures of welfare outcomes for individual animals. Observations and interpretations of behavior are the most widely used outcome-based measures of animal welfare. They commonly serve as a diagnostic tool from which practitioners make animal welfare decisions and suggest treatments, yet errors in data collection and interpretation can lead to the potential for misdiagnosis. We describe the perils of incorrect welfare diagnoses and common mistakes in applying behavior-based tools. The missteps that can be made in behavioral assessment include mismatches between definitions of animal welfare and collected data, lack of alternative explanations, faulty logic, behavior interpreted out of context, murky assumptions, lack of behavior definitions, and poor justification for assigning a welfare value to a specific behavior. Misdiagnosing the welfare state of an animal has negative consequences. These include continued poor welfare states, inappropriate use of resources, lack of understanding of welfare mechanisms and the perpetuation of the previously mentioned faulty logic throughout the wider scientific community. We provide recommendations for assessing behavior-based welfare tools, and guidance for those developing tools and interpreting data.
... Therefore, we recommend further research with a wider range of enrichment devices, such as those described in previous studies of turtles (Therrien et al. 2007). We recommend specifically for marine turtles (Bluvias & Eckert, 2010), as well as for other reptiles (Mohan-Gibbons & Norton 2010; Bashaw et al. 2016), that various enrichments including but not limited to visual (e.g. mirrors, images), olfactory (e.g. ...
Article
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Wild sea turtles that are admitted to turtle hospitals and rehabilitation centers suffering from illnesses and injuries may be held for extended periods of months to years, until they are recovered and ready for release back to the wild. During this time, natural behaviors may be limited, potentially adversely affecting the long-term rehabilitation success, however, little research has been carried out on the behavior of hospitalized sea turtles. Here we report that environmental enrichment can be an effective means of encouraging natural behaviors in turtles in hospital/rehabilitation and aquarium settings, but find that enrichment should be monitored and tailored to individual turtles to achieve positive results.
... For example, mammals were the subject species for 75% (84/112) of the identified literature [49,50]. Of these studies, the Orders of Carnivora [50][51][52][53][54][55][56][57], Cetacea [10,46] and primates [18], particularly chimpanzees (Pan troglodytes) [58][59][60][61] were the most commonly studied groups. While reptile [62][63][64], bird, fish [65] and invertebrate [66,67] species appeared in some studies, they were in the minority overall. ...
Article
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Behavioral diversity is a commonly used tool used to quantify the richness and evenness of animal behaviors and assess the effect of variables that may impact an animal’s quality of life. The indices used in behavioral diversity research, and the study subjects, have not been formally reviewed. This paper aims to identify which indices are being used in behavioral diversity research, and under which scenarios, and uncover novel indices from other disciplines that could be applied to behavioral diversity. To investigate the techniques and species investigated in behavioral diversity literature, a Web of Science literature search was conducted. Two methods: behavioral richness and the Shannon–Wiener index, were the most frequently used indices, whereas the Behavioral Variability index featured rarely. While a range of species appeared in the behavioral literature, mammals were the most frequently studied Class, whereas amphibians did not feature in any papers. There are several diversity indices which did not feature in behavioral diversity including Simpson’s index, and Chao. Such indices could be used to better understand animal behavioral study outputs or be used to estimate the number of ‘unobserved’ behaviors that an animal may express. Future studies could therefore extend beyond the Shannon–Wiener and richness indices.
... Recent work into reptile welfare has shown promising applications for husbandry and care in captive settings (e.g., pets, zoo specimens, etc.). For instance, providing enrichment has been shown to reduce escape behavior in captive turtles (Bannister et al., 2019) and increase welfare for leopard geckos (Bashaw et al., 2016). Moreover, snakes have shown preference for enriched over non-enriched habitats (Hoehfutner et al., 2021). ...
Article
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The study of animal personality is a growing field that has applications for welfare of animals living in captive settings. We measured personality traits (activity, exploration, and neophobia) in Texas horned lizards (Phrynosoma cornutum) living in human care before they were released to their natal habitat as part of a headstart program. We found evidence of consistent inter-individual differences in activity and exploration, but not neophobia. We also identified a positive correlation between activity and exploration, such that more active lizards were also more likely to explore a novel environment. These results suggest that Texas horned lizards have individual differences in response to their environment, which can inform husbandry decisions. Extensions of this work could also have implications for conservation of Texas horned lizards and for headstart programs focused on reptiles.
... Recently, Nagabaskaran et al. has shown that zoo-housed snakes (Fig.5 ) are better able to perform their natural behaviours when living in an enriched environment [17], while Bashaw et al. found an improvement in captive leopard gecko welfare with the provision of different types of enrichment. The geckos reportedly responded to enrichment in a manner similar to carnivorous mammals [1]. ...
Conference Paper
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This workshop is focused on the design of novel kinds of environmental enrichment for zoo-housed reptiles, using technology to support the development of interactive systems and devices for capturing data. Participants will work virtually in small groups to ideate, reflect on and develop concepts, using a ZooJam approach, which is similar to a game jam. Briefs for participants may include lizards, snakes, turtles and crocodilians.
... There are many definitions of environmental enrichment (EE) within the literature, but EE is commonly described as a technique designed to enhance the quality of life in captive and domestic animals by providing additional and temporary environmental stimuli to promote psychological and physiological wellbeing [1][2][3]. EE has been shown to be beneficial to the wellbeing of species including rats [4], pigs [5], cats [6] and geckos [7]. ...
Article
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Environmental enrichment (EE) can be used to enhance the environment of various animals. The aim of this pilot study was to determine the effects of seven EE activities (Bonding, Bubble machine, Conspecific play, Interactive toy, Playhouse, Stuffed food toy and Tug play) on dog behaviour, pre- and post-EE for dogs housed in an office environment during training as part of an assistance dog training programme. EE activities resulted in a significant increase in the frequency of relaxation behaviours (p < 0.01) and a significant reduction in alert (p < 0.01) and stress behaviours (p = 0.02). Results suggest various benefits of the different activities with Conspecific Play and Playhouse activities having the greatest overall positive behaviour change when compared to the other activities. The food-based EE activities (Interactive toy and Stuffed food toy) had the least behaviour change of all the activities provided. Findings will be of interest to pet owners, animal rescue centres, dog trainers and working dog organisations.
... In the last decade, many studies on the foraging behavior and daily activities of geckos have been carried out (Tawa et al., 2014;Haley & Blackshaw, 2015;Bashaw et al., 2016;Baxter-Gilbert et al., 2021). A study on Gekko japonicus shows that the distribution of daily locomotor activity of this species is affected by temperature (Tawa et al., 2014). ...
Article
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To understand the role of the flat-tailed gecko on pest control in urbanized areas, we observed the foraging behavior and daily activity of H. platyurus. It is one of the house geckos easily found but more studies on their behavior are still lacking. The observation was conducted between 14−27 May 2021, for 18 hours starting from 09.00 to 03.00 WIB using the ad libitum sampling method. Our result suggests that the foraging behavior was found almost every hour of observation, which is strongly influenced by relative humidity and insect abundance. This gecko was observed as a sit-and-wait predator or passively searching for prey. Our observation also indicated that this species has potential to control one of the household pests, the adult ants (alates). Hopefully, this study contributed to the understanding of the foraging behavior of the flat-tailed gecko. However, more studies are needed for better understanding of foraging behavior in the flat-tailed gecko.
... The competing stimuli framework is used in ABA to identify which items or activities effectively reduce problem behaviors by offering alternative sources of reinforcement [118,119]. By monitoring an individual animal's (or group's) enrichment use and problem behavior across different enrichment conditions using within-subjects designs, behavior analysts could make datadriven decisions regarding the best implementation of a variety of different types of potential enrichment items or events [75,80,82,117,120,121]. ...
Article
Full-text available
The modern zoo has been associated with two major behavioral welfare advances: (a) the use of training to increase voluntary husbandry care, and (b) the implementation of environmental enrichment to promote naturalistic behaviors. Both practices have their roots in behavior analysis, or the operant conditioning-centered, reward-based approach to behavioral psychology. Operant conditioning served as the foundation for the development of reinforcement-based training methods commonly used in zoos to make veterinary and husbandry procedures easier and safer for animals and their caregivers. Likewise, operant conditioning, with its focus on arranging environmental antecedents and consequences to change behavior, also provided a framework for successful environmental enrichment practices. In this paper, we outline the key individuals and events that shaped two of the cornerstones of the modern zoo: (1) the emergence of reward-based husbandry training practices, and (2) the engineering of environmental enrichment. In addition, we (3) suggest ways in which behavior analysis can continue to advance zoo welfare by (i) expanding the efficacy of environmental enrichment, (ii) using within-subject methodology, and (iii) improving animal-visitor interactions. Our goal is to provide a historical and contextual reference for future efforts to improve the well-being of zoo animals.
... The competing stimuli framework is used in ABA to identify which items or activities effectively reduce problem behaviors by offering alternative sources of reinforcement (Haddock & Hagopian, 2020). By monitoring an individual animal's (or group's) enrichment use and problem behavior across different enrichment conditions using within-subjects designs, behavior analysts could make datadriven decisions regarding the best implementation of a variety of different types of potential enrichment items or events (Alligood et al., 2017;Bashaw et al., 2016;Carlstead et al., 1991;Fernandez & Timberlake, 2008;Markowitz et al., 1995;Sanders & Fernandez, 2020). ...
Preprint
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The modern zoo has been associated with two major behavioral welfare advances: (a) the use of training to increase voluntary husbandry care, and (b) the implementation of environmental enrichment to promote naturalistic behaviors. Both practices have their roots in behavior analysis, or the operant conditioning-centered, reward-based approach to behavioral psychology. Operant conditioning served as the foundation for the development of reinforcement-based training methods commonly used in zoos to make veterinary and husbandry procedures easier and safer for animals and their caregivers. Likewise, operant conditioning, with its focus on arranging environmental antecedents and consequences to change behavior, also provided a framework for successful environmental enrichment practices. In this paper, we outline the key individuals and events that shaped two of the cornerstones of the modern zoo: (1) the emergence of reward-based husbandry training practices, and (2) the engineering of environmental enrichment. In addition, we (3) suggest ways in which behavior analysis can continue to advance zoo welfare by (i) expanding the efficacy of environmental enrichment, (ii) using within-subject methodology, and (iii) improving animal-visitor interactions. Our goal is to provide a historical and contextual reference for future efforts to improve the well-being of zoo animals.
... Environmental enrichment can be defined as stimuli and/or events that are added to or modify an animal's environment and result in some measurable improvement in behavioral and/or physiological wellbeing/welfare (Fernandez et al., 2021a;Fernandez & Timberlake, 2008;Hoy et al., 2010;Mellen & MacPhee, 2001;Newberry, 1995;Shepherdson, 1998). Some examples of enrichment include the use of foraging devices and feeding schedules, both automated and non-automated (Andrews & Ha, 2014;Bashaw et al., 2016;Fernandez, 2010;Fernandez, 2021;Shepherdson et al., 1993), changes in enclosure presentations, including choice between enclosures Coe, 2004;Sherwin et al., 1999), and the presentation of auditory, olfactory, and/or visual stimuli Fernandez & Timberlake, 2019a;Graham et al., 2005;Platt & Novak, 1997;Wells & Irwin, 2008). ...
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Husbandry training and environmental enrichment are both important advancements associated with current behavioral welfare practices. Additionally, the use of training procedures has been proposed as a form of enrichment, with the implication that training can produce beneficial behavioral welfare results. This paper examines the concept of training as enrichment through three distinct ways training procedures could enrich: (1) training facilitates enrichment usage, (2) training modifies interactions, conspecific or otherwise, and (3) training expands behavioral repertoires. Within each category, the paper focuses on past research that provides empirical support for training functioning as enrichment, as well as related areas of research that provide additional evidence. Previous studies support the claim that training is enriching, with additional research necessary to better understand how prevalent and under what conditions training procedures function as enrichment. Future training research should examine these potential enrichment effects, including methodology that allows for comparisons to traditional enrichment, the use of welfare diversity/variability indices, and the effects of learning on trainers and trainees alike.
... In zoological park settings, welfare assessments have become more frequent because of general public concerns and zoo professionals emphasising the need to measure the welfare of their animals objectively and scientifically [15]. Several of those assessments include and use behavioural diversity indexes in a variety of zoo animal species: for instance, in elephants (Loxodonta africana, Elephas maximus) [16], reptiles [17,18], cheetahs (Acinonyx jubatus) [19], gentoo penguins (Pygoscelis papua) [20], flamingos (Phoenicopteridae) [21], lions (Panthera leo) [22], aardvarks (Orycteropus afer) [23] and red foxes (Vulpes vulpes) [24], among others. Studies showed that behavioural diversity is influenced by environmental enrichment [7,25], as described in African lions (Panthera leo) [26], in Australian fur seals (Arctocephalus pusillus doriferus) [27] and in European wolves (Canis lupus lupus) [28]. ...
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In the recent past, animal welfare studies have tried to determine the best animal welfare measures and indicators. Expression of behavioural diversity is considered a potential positive welfare indicator, and to the authors’ knowledge, it has not been validated nor studied in cetaceans. For the first time, a behavioural diversity study on bottlenose dolphins (Tursiops truncatus) groups was conducted at six European facilities. The study was carried out by the animal care staff, biologists and veterinarians and included 54 dolphins housed in several group compositions at the different participating facilities. The goal of our study was to analyse behavioural diversity in bottlenose dolphins at the group level to investigate how particular factors might impact the diversity of behaviours within the group and to discuss its implications for dolphin welfare assessments. Eight factors (i.e., “observer location”, “number of individuals”, “age class”, “sex”, “social grouping”, “presence/absence of leading male”, “presence/absence of visitors” and “enrichment provision”) impacted the behavioural diversity of the observed groups, while no significant impact of the factors “time of day” and “activity before/after observation” could be found. Our study showed the feasibility of this kind of approach for cetaceans under professional care and the relevance to considering this parameter in dolphin welfare studies, despite certain limitations that warrant further research.
... Those studies that have been carried out have generally found that enrichment is beneficial (e.g. Chelonia, Therrien et al., 2007;Case et al., 2005;Mehrkam andDorey, 2014 andlizards Phillips et al., 2011;Hennig and Dunlap, 1978;Londoño et al., 2018;Bashaw et al., 2016). There are very few studies investigating snake welfare (e.g. ...
Article
There is a wealth of evidence demonstrating the benefits of environmental enrichment across a range of different animal species. However, there is comparatively little such research into the effect of enrichment provision on captive reptiles. The aim of this study was therefore to ascertain if an increase in environmental complexity was beneficial to the behaviour and welfare of corn snakes (Pantherophis guttatus). The study used a combination of behavioural observations in the home enclosure, behavioural tests of anxiety, and a preference test. The snakes used the enrichment when it was available to them and enriched snakes showed changes in general behaviour reflective of improved welfare. However, the anxiety tests revealed few effects of enrichment provision on performance. In contrast, the snakes exhibited a strong preference for the enriched enclosure when given a choice. These findings suggest that the provision of environmental complexity to the enclosure was beneficial to the behaviour and welfare of captive corn snakes. We therefore recommend enrichment should be used when keeping captive snakes.
... Environmental enrichment can be defined as stimuli and/or procedures that are added to or modify an animal's environment and result in some measurable improvement in the behavioural and/or physiological well-being (i.e., welfare or wellness) of an exhibited animal [10][11][12][13]. Some examples include the use of foraging devices and feeding schedules, both automated and non-automated [14][15][16][17][18][19][20], changes in enclosure presentations, including choice between enclosures [21,22], the presentation of auditory, olfactory, and/or visual stimuli [23][24][25][26][27], and the use of operant conditioning and various other animal training practices [28,29]. In addition to the welfare benefits for enriched animals, increased animal activity has also been correlated with increased visitor attention to those exhibited animals [30][31][32][33][34][35]. ...
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Penguins are considered among the most popular animals for zoo and aquarium visitors to observe. Swimming is considered a desirable activity, both for the visitor experience and the welfare of the penguins. However, little is known about the amount of time exhibited penguins spend swimming, or how such swimming is related to regular feeding events. We examined the effects of introducing live prey in the form of trout on 22 Humboldt penguins living at the Woodland Park Zoo. Of primary interest was how the live feeds changed (1) daily and hourly swimming activity, and (2) variability in enclosure use. We hypothesized that the live feedings would increase swimming activity prior to and during the delivery of the live trout, as well as create an overall increase in total swimming activity for live feed days compared to non-live feed days. We also predicted that the penguins would be more likely to use the entire exhibit around these live feeds, since they are likely to chase fish throughout the exhibit. Penguins did show an increase in swimming activity in the hour prior to and during the live feed, with a small decrease in swimming activity following the live feed when compared to non-live feed days. There was also a more than 30% increase in the total swimming activity for live feed days when compared to all other non-live feed days. In addition, a single measure of variability in enclosure use (entropy) showed greater overall enclosure use for the live feed days compared to the non-live feed days. These results demonstrate that live fish can be a useful way of enriching the behavioural welfare of Humboldt penguins.
... One purpose of enrichment is to increase naturalistic behaviors of exhibited animals through the introduction of stimuli and/or changes in feeding opportunities. Included among these have been the use of particular food presentations with bears (Andrews & Ha, 2014;Carlstead, Seidensticker, & Baldwin, 1991;Law, Boyle, Johnston & MacDonald, 1990), and with felids (Lyons, Young, & Deag, 1997;Shepherdson, Carlstead, Mellen, & Seidensticker, 1993), effects of acoustic "prey" on African leopards (Markowitz, Aday, & Gavazzi, 1995), inedible, manipulable objects given to zoo and aquarium animals (Altman, 1999;Bashaw, Gibson, Schowe, & Kucher, 2016;Clark, Davies, Madigan, Warner, & Kuczaj, 2013), enclosure manipulations, including choice between enclosures (Carlstead, Brown, & Seidensticker, 1993;Sherwin, Lewis, & Perry, 1999), and access to conspecifics or stimuli associated with conspecifics (Bourgeois & Brent, 2005;Mills & Riezebos, 2005). ...
Conference Paper
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The modern zoo has brought about two major advances in the behavioral welfare of their exhibited animals: (a) The use of environmental enrichment to promote naturalistic behaviors and (b) the use of training to improve voluntary husbandry care. Whereas training itself has been talked about as an effective enrichment strategy, little has been done to combine training procedures with enrichment. Typically, enrichment is treated as a trial and error process, where potential enrichment items or procedures are cycled through until successful enrichment is found. The use of shaping or other training techniques has seldom been documented to increase engagement with possible enrichment items or procedures. The following study examined the possibility of combining training and enrichment to produce continued interactions with enrichment devices. Two species of penguin, Magellanic and southern rockhopper penguins, were studied. Two measures were taken: Time spent swimming and contact with enrichment devices. The enrichment devices could be manipulated by placing fish within and hanging out of each device. During baseline sessions, no hits to either device were observed. During training sessions, several hits were recorded when fish were in the devices and overall swimming time increased during these conditions. When baseline was reintroduced without fish in the devices, contact with the enrichment devices rapidly declined and swimming time for the rockhopper penguins decreased. When the devices were reintroduced with fish but without training, the greatest number of enrichment device contacts and the highest percentage of time spent swimming were observed for the rockhopper penguins.
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Novelty recognition helps organisms identify changes over time. Studies to date have usually involved mammals, particularly rodents. We explored leopard geckos’ (Eublepharis macularius; Experiment 1) and tiger salamanders’ (Ambystoma tigrinum, Experiment 2) sensitivity to spatial and object novelty. We used an exploratory paradigm adapted from rodents where time spent near objects in an open-field box was compared. Subjects first habituated to three objects. To evaluate spatial novelty recognition, one object was moved to a new location. Subjects again habituated to the objects’ locations. To evaluate object novelty recognition, one object that had not been moved earlier was replaced with an unfamiliar object. Results indicated when one object was moved to a new location, geckos and salamanders spent more time near that spatially-displaced object. Additionally, when a familiar object was replaced with a new object, geckos and salamanders spent more time near the substituted object. These results suggest geckos and salamanders recognized changes in objects’ identities and locations. Geckos and salamanders acted differentially depending on familiarity in both spatial and object domains. These results support attempts to include lesser-studied species in our efforts to characterize cognition.
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The aim of this study was to use behavioural observations to assess the welfare of the red-necked pond turtles (Mauremys nigricans) kept in a zoo. In 2000, red-necked pond turtles were put on the critically endangered list. Today, the species appears to be extinct in the wild. The welfare of captive populations of the species will have an important impact on their survival. Due to unusual aspects of reptile biology and a lack of monitoring standards, the main criteria available for welfare assessment for these animals may be behavioural. Based on the results of this study, it can be inferred that the welfare of the observed turtles has been moderately well-preserved; however, the artificial conditions created by humans are not able to fully satisfy the behavioural needs of the studied animals.
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All animals must move efficiently throughout their world. However, the mechanisms through which they accomplish this potentially vary among species. Previous work exploring the use of feature information and geometric information in movement through space has indicated that geometric information is commonly used and that some species sometimes also use feature information. Here, I investigated if a cold-blooded species, leopard geckos (Eublepharis macularius), would use geometric and/or feature information. In training, geckos learned to move to a correct corner within the box with a distinctive feature. In test when only geometric information was available, geckos chose either their assigned corner or its geometric opposite. In another test when feature information conflicted with geometric information, geckos did not use feature information and instead made choices consistent with using geometric information. This suggests geckos used geometric information preferentially to feature information in this experiment after both had been available throughout training when they were placed in conflict.
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Crocodile monitors are impressive canopy dwellers; these large lizards are an apex predator of the tropical forests of the island of New Guinea. Being highly active and energetic animals, they offer an interesting option for a tropical habitat in any zoological institution. Moreover, this charismatic animal is an excellent ambassador to highlight the rampant habitat destruction in their native forests, the threats posed by the illegal and unsustainable wildlife trade, and the need for further conservation efforts. However, crocodile monitors are considered difficult to manage and breed in captivity. Furthermore their lifespan in captivity is presumably shorter than their wild counterparts. Therefore only a few zoological institutions dare to include them in their collection plans. Over recent years, substantial efforts have been placed in improving the captive management of this species resulting in new research and breeding successes that indicate an overall improvement of the knowledge of this species. These EAZA Best Practice Guidelines were developed with the objective of improving the evidence-based knowledge of this species and provide the most comprehensive and up-to-date information for Zoological Institutions to ensure their animals have access to the best care. The aspirational aim of this guide is to provide an overview of the critical components that need to be considered when keeping a large arboreal tropical lizard, to guarantee positive welfare experiences and correct physical development. By doing so, we expect to increase the breeding rate and lifespan in captivity and thus reduce the need or desire to remove this species from the wild. Improved understanding and appreciation of this species in captivity will also allow zoos to play an increased role in supporting and informing ex situ conservation efforts for this species. Additionally, we aim to raise the profile of the species as a suitable candidate for tropical exhibits in zoos across the EAZA members.
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Environmental enrichment is a strategy used to improve the welfare of animals under human care. While enrichment techniques for mammals and birds have been studied extensively, reptilian enrichment has received less attention. There has been an increase in enrichment programs for reptiles in zoological institutions, however many are not accompanied by behavioral studies. Detailed recording of behavioral responses to enrichment is necessary to assess the efficacy of the enrichment type and to determine its utility in various settings. In this study, 18 snakes of multiple species, from two Families (Colubridae, Pythonidae), were exposed to four enrichment types (Humid Hide, Olfactory, Climbing, Suspended Hide). Baseline recordings were conducted prior to the introduction of enrichment. Snakes were recorded for two hours after introduction of each item. Five behavior types were identified based on baseline videos: tongue flicking, climbing, hiding, interacting with transparent boundaries, and utilizing non-enrichment items. Interacting with transparent boundaries was classified as an undesirable behavior, while the other four behaviors were classified as desirable. Changes in climbing and tongue flicking behaviors were noted with introduction of each item- these changes were not statistically significant. The increase in these behaviors may indicate clinical importance, and shows that snakes under human care respond to environmental enrichment. As some snakes showed a reduction in undesirable behaviors when compared to baseline conditions, this may suggest increased welfare during times when enrichment is offered. The extent to which these results can be applied to other species merits further study.
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Providing enrichment that expands the range of behavioral opportunities associated with food acquisition and environmental exploration is an important contributing factor to the well-being of zoo animals. These behaviors can be difficult to promote in carnivores, given their foraging strategies and the logistical, ethical, and financial challenges of providing live prey. In this study, we introduced a novel feeding enrichment to Jacksonville Zoo and Gardens' five adult American alligators (Alligator mississippiensis) in an attempt to simulate a live prey organism within the exhibit and promote natural hunting behaviors like chasing and lunging, as well as increase daily activity levels. The enrichment promoted some behavioral goals for two of the alligators, but it did not promote behavioral goals for the other three alligators. This could have been due to a variety of factors including an existing dominance hierarchy amongst the group's females and the resulting spatial distribution of individuals across a habitat with only one water feature. Our results suggest that female alligators may carve out territories and avoid overlapping space usage with other females during the warmest months of the year. Given the outcomes and limitations of this enrichment strategy, we provide recommendations for this group specifically as well as future enrichment efforts in the general captive crocodilian population.
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Zoological institutions use environmental enrichment to increase opportunities for animals to engage in species-appropriate behavior. In these facilities, enrichment for giraffe typically consists of different types of feeders to increase the percentage of time spent foraging. The current study explored the use of scent enrichment as a way to increase exploration, activity levels and space use in zoo-housed Rothschild giraffe. Study one investigated the preferences of individual giraffe to six scents while study two investigated how scent enrichment affected behavior when applied in their main exhibit. Results suggest that there are individual differences in scent preference in giraffe and that scents can be used to decrease inactivity and alter exhibit utilization in the short-term. If provided in appropriate areas, depending on the species, scent enrichment may promote a better experience for zoo visitors by bringing the animals closer to the viewing areas while benefiting the animals. Future research is still needed to better understand the effects of olfactory enrichment on zoo animals.
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The behaviour and body temperatures of the bearded dragon (Pogona vitticeps) were recorded during periods with handling and non-handling intervals. Differences in perching and hiding were observed after the animals were handled but basking and locomotory activity remained almost constant. The observed differences in behaviour appeared to have no influence on either set point or variance in body temperatures.
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Reptiles and amphibians have been neglected in research on cognition, emotions, sociality, need for enriched and stimulating environments, and other topics that have been greatly emphasized in work on mammals and birds. This is also evident in the historic lack of enriching captive environments to reduce boredom and encourage natural behavior and psychological well-being. This paper provides those responsible for the care of reptiles and amphibians a brief overview of concepts, methods, and sample findings on behavioral complexity and the role of controlled deprivation in captive herpetological collections. Most work has been done on reptiles, however, and so they are emphasized. Amphibians and reptiles, though not admitting of easy anthropomorphism, do show many traits common in birds and mammals including sophisticated communication, problem solving, parental care, play, and complex sociality. Zoos and aquariums are important resources to study many aspects of these often exotic, rare, and fascinating animals, and rich research opportunities await those willing to study them and apply the wide range of methods and technology now available. (c) 2013 Elsevier B.V. All rights reserved.
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When zoo-housed animals have choice over aspects of their environment, and are able to exercise control over interactions with their surroundings, welfare can be improved and exhibits' value to the zoo increased. Reptiles and amphibians are not common subjects in enrichment studies yet their demanding captive requirements suggest a need for enclosure diversity and biologically sound enrichment programmes. As popular captive subjects, such animals are readily available for potential research projects that investigate behaviour, welfare and effects of enclosure design. Undergraduates on animal science courses that undertake a research-led dissertation or similar projects can collect data on such species that, if collected under a robust methodology, can be used to inform future husbandry decisions. This paper discusses three small-scale studies (on two reptile species and one amphibian species) that were designed to improve husbandry and welfare. The aim of the paper is to show that undergraduate projects, properly managed, can have a positive impact on overall day-today exhibition and management of these species. Results from these projects have shown that small changes to enclosure design can have a beneficial impact on activity patterns, and that overall enclosure design can help display the animals in a more interesting way to visitors. Potentially, the animal welfare benefits of enriched setups can be passed on to zoo visitors in the form of a more engaging, exciting and educationally relevant zoo experience.
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We tested the hypothesis that thermoregulation increases growth rate in nocturnal Lizards. Leopard geckos (Eublepharis macularius) maintained from hatching at 25 C grew at a rate of 0.11 g/day, while geckos allowed to thermoregulate at preferred body temperatures (30 C for 13.5 h per day) grew 1.5 times as fast (0.16 g/day). Long-term thermal treatment had a significant reverse acclimation effect on preferred body temperature (T-p): T-p was 1.2 C lower in thermoregulatory individuals than in Chose kept at 25 C. Feeding and time of day also had significant but minor effects on T-p. Despite their nocturnal ecology, leopard geckos seem to be typical among Lizards in requiring a diurnal heat source for maximal growth. This result provides a physiological explanation for the observation that some nocturnal lizards thermoregulate in burrows during the day, and may have implications for the biogeography of nocturnal ectotherms.
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The concept of the human–animal relationship (HAR) is widely used in farm animal research to describe the outcome of the different qualities and quantities of interaction between stockpersons and the animals in their care. Thus, negative, positive or neutral HARs may result from the effect of mostly negative (e.g. rough handling), neutral (e.g. no handling) or positive (e.g. gentle handling) interactions. In this paper the concept is applied to zoo animals in an attempt to provide a model not only of HARs between zoo animals and keepers, but also between zoo animals and unfamiliar people, primarily the visiting public. Behavioural responses of animals to zoo visitors are inconsistent both within and between taxa, and the history of interactions the individual animal has experienced, and hence the HARs it has developed, may be one of the variables that leads to this inconsistency. The model starts, like the farm animal models, with the animals’ fear of humans, which is itself dependent upon species. The subsequent history of interactions the animal experiences, both with familiar and unfamiliar people, then determines the animal's HAR, which in turn influences the way the animal responds to people. There are currently insufficient data to test the model, but predictions of the model are identified here which could be used to test it.
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Gekkonid lizards are shown to have well-developed nasal chemical senses. It is argued that they are unique among squamates so far studied in the degree of their olfactory (as opposed to vomeronasal) development. This contention is supported by evidence from the brain, nasal capsule, tongue, and experimental studies of behaviour. Limited evidence suggests that olfaction functions in food-finding and predator detection; vomerolfaction during investigation of novel stimuli and in reproduction. The conception of gekkonids as members of a ‘visual Ascalabota’ is not supported by these findings. Olfactory specialization makes geckos ideal subjects for tests of the Cowles and Phelan hypothesis of olfactory function and suggests that they might be better subjects than snakes for future studies of dual olfactory form, function and evolution in a nonmammalian lineage.
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The influence of an environmental enrichment programme on the searching behaviour of separate groups of male and female bush dogs at Edinburgh Zoo was evaluated. The enrichment programme involved hiding food in specially constructed wood-piles and other appropriate places in the bush dogs' enclosures. Behavioural data were recorded morning and afternoon for 20 consecutive experimental days and were compared to pre- and post-enrichment programme data, representing basal conditions. Data were collected over a 10-day period for both pre and post enrichment phases. Activities were recorded under seven behavioural categories. There was no significant difference between sexes in the proportion of time spent performing searching behaviour so data were pooled. The enrichment programme appeared to cause an increase (P < 0.01) in searching behaviour from initial basal conditions of 2.7 per cent to 6.1 per cent of total recorded data points. There was a subsequent decrease in searching behaviour (P < 0.01) to 2.5 per cent when basal conditions were reinstated. All dogs showed increases in searching behaviour when enrichment and basal data were compared. The effectiveness of the enrichment programme in terms of increasing the proportion of time spent in searching behaviour showed a significant decline (P < 0.005) over time, probably relating to the dogs increasing proficiency at finding food. It is suggested that the enhanced levels of searching behaviour represent an improvement in welfare.
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A study was conducted over 24 days to evaluate the effects of three environmental enrichment techniques (frozen balls of ice containing fish, various scents, hanging logs) on four captive African lions (Panthera leo). Behavioural data on activity level and behavioural diversity were collected daily during a baseline and an enriched session. All enrichments produced positive changes in behaviour. Enrichment was also associated with increased use of space by the lions. The enrichment techniques evaluated in this study each produced distinct and positive changes in behaviour thus reinforcing the need for variety to be exercised in captive enrichment programmes. Providing different enrichments allows animals to perform a greater range of behaviours, become more active in captivity, and will decrease the likelihood of habituation to certain enrichment items. Environmental enrichment should be a part of any management protocol for animal welfare and health.
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Spatial cognition is predicted to be a fundamental component of fitness in many lizard species, and yet some studies suggest that it is relatively slow and inflexible. However, such claims are based on work conducted using experimental designs or in artificial contexts that may underestimate their cognitive abilities. We used a biologically realistic experimental procedure (using simulated predatory attacks) to study spatial learning and its flexibility in the lizard Eulamprus quoyii in semi-natural outdoor enclosures under similar conditions to those experienced by lizards in the wild. To evaluate the flexibility of spatial learning, we conducted a reversal spatial-learning task in which positive and negative reinforcements of learnt spatial stimuli were switched. Nineteen (32%) male lizards learnt both tasks within 10 days (spatial task mean: 8.16 ± 0.69 (s.e.) and reversal spatial task mean: 10.74 ± 0.98 (s.e.) trials). We demonstrate that E. quoyii are capable of flexible spatial learning and suggest that future studies focus on a range of lizard species which differ in phylogeny and/or ecology, using biologically relevant cognitive tasks, in an effort to bridge the cognitive divide between ecto- and endotherms.
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Giving captive animals the opportunity to interact with objects in a “playful” manner is often considered a method of environmental enrichment. However, the occurrence of play in nonavian reptiles is controversial and poorly documented. Similarly, the role of environmental enrichment in fostering psychological well-being in reptiles has been little studied. For several years, an adult, long-term captive, Nile soft-shelled turtle, Trionyx triunguis, at the National Zoo (Washington, D.C.), was provided objects such as balls, sticks, and hoses in an attempt to reduce self-mutilation behavior. The turtle spent considerable time with the objects, and the level of self-mutilation behavior decreased greatly over many months. Video recordings made in various contexts were analyzed in detail, and an ethogram of this turtle's behavior was developed. The turtle interacted with the objects (e.g., basketball, hose, stick) for 20.7% of the time it was observed and was active for 67.7% of the time. Both figures are unusually high for any animal, especially a turtle. The relative lack of play in ectothermic reptiles is supported by the surplus resource theory of play, which considers the joint effects of parental care, metabolism, endothermy, and arousal in providing the context in which playfulness could be manifested and promoted in vertebrate evolution. The existence of vigorous playlike behavior in a member of an ancient reptilian lineage indicates that, in the right circumstances, object play can be performed by reptiles and that having the opportunity to do so may be beneficial in captivity. © 1996 Wiley-Liss, Inc.
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Although behavioral studies have been conducted at zoos and aquaria for years, documentation concerning the effectiveness of environmental enrichment has dealt primarily with terrestrial animals and marine mammals. Few enrichment studies have been conducted on reptiles. For this study, behavioral observations were made on four captive sea turtles (three loggerhead, Caretta caretta, and one blind green, Chelonia mydas) with enrichment present and absent. Enrichment devices were modified for the special needs of the blind turtle. Behaviors were classified as Resting, Pattern Swimming, Random Swimming, Focused Behavior, Aggression, Hiding, Orientation, and Noncategorized Behavior. It was hypothesized that, when enrichment was present, a decrease in Resting and stereotypic Pattern Swimming would be seen along with an increase in Random Swimming and Focused Behavior. It was found that, when no enrichment devices were present, 77% of the turtles' time was spent in Resting and Pattern Swimming. When enrichment devices were provided, 88% of their time was spent in Random Swimming and Focused Behavior with only 8% spent in Pattern Swimming and Resting. Statistically, there were significant increases in Random Swimming (three of the four turtles) and Focused Behavior (4/4) and significant decreases in Resting (3/4) and Pattern Swimming (3/4) when enrichment devices were present. These results suggest that environmental enrichment is as effective with marine reptiles as has been found with other animals and should be encouraged for all captive sea turtles. Zoo Biol 26:407–416, 2007. © 2007 Wiley-Liss, Inc.
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The zoo scientific community was among the first to focus attention on captivity-induced stereotypic behaviors, their causes, and methods of eradication. Environmental enrichment has emerged recently as the main husbandry tool for tackling this problem. An increasing number of research publications have attempted to evaluate the effectiveness of enrichment in reducing stereotypic behavior and to develop further concepts to explain how effective enrichment works. A review and meta-analysis of this literature indicates that enrichment is a successful technique for reducing stereotypic behavior in zoo animals. Enrichment was associated with significant reduction in stereotypy performance about 53% of the time. Published enrichment and stereotypy research is lacking for most zoo species, with most studies on large, charismatic, and often endangered species, but it is unclear whether stereotypies are more prevalent in these species. In addition, problems with scientific methods and data presentation, quantitatively detailed in this work, severely limit the conclusions drawn from zoo research. Further understanding of what kinds of enrichment works and what doesn't will require greater attention to experimental design, sample size, statistical analysis, and better descriptions of enrichment properties and the form of stereotypy. We recommend that future studies focus on increasing sample size (e.g., through multi-institutional studies), appropriate repeated measures design (e.g., with multiple baseline and experimental phases), providing full statistical information about the behavioral changes observed (including standard error), and ultimately the development of a predictive science for enrichment, stereotypies, and wellbeing. Zoo Biol 0:1–20, 2005. © 2005 Wiley-Liss, Inc.
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Olfactory stimuli are frequently integrated into zoo enrichment programs. This ‘olfactory enrichment’ can stimulate reproduction or naturalistic behaviour, enhance enclosure exploration, or reduce inactivity. However, not all scents achieve their desired goals, and can in fact bring about undesirable behaviour such as increased levels of stereotypy. Few attempts have been made to quantify the impact of introducing olfactory stimuli to zoo enclosures, and there are inherent difficulties when designing, implementing and evaluating olfactory enrichment. Firstly, it is difficult without appropriate chemical analyses to anticipate what information a scent conveys, and therefore whether it will be received as an excitatory or aversive stimulant. Second, more practical difficulties are encountered. Consideration needs to be given to (i) the choice of scent used, its relevance and motivation, (ii) how to present the scent in time and space, (iii) individual variation in response rates and neophobia (fear of novelty) to scents, and finally (iv) the health implications linked to the use of olfactory stimuli. This paper reviews the olfactory stimuli used in zoos as enrichments and their reported effects. Practical suggestions are made to encourage and stimulate more empirical quantification of olfactory stimulation in zoo animals.
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Enrichment aims to improve captive animals' welfare by enhancing their environments. Two of the struggles associated with measuring welfare are identifying when animals' needs are being met or surpassed and identifying how individual differences play a role in these outcomes. Using a group of related Guyanese squirrel monkeys, we studied changes in five welfare indicators under different environmental conditions. Manipulating food presentation, walkways, and toys, we created five enrichment levels ranging from just above USDA standards to considerably more complex than the animals' normal housing. At the end of each level, a novelty test was performed in which an unfamiliar woman entered the enclosure and offered food. Changes in behavior as a function of enrichment condition were analyzed using a repeated-measures MANOVA. Compared to baseline, less enrichment consistently increased negative welfare indicators (abnormal behavior, aggression, and negative responses to the novelty test), while more enrichment sometimes decreased these indicators. Positive welfare indicators were less consistently related to enrichment, but positive response to the novelty test did increase somewhat in the most enriched condition. Across conditions, rank correlations revealed that individuals had highly consistent individual differences in positive responses to novelty and somewhat consistent individual differences in rates of aggression. The goal of the enrichment and the species, sex, and individual animals to be enriched should be considered when selecting a welfare indicator, and facilities measuring animal welfare should study changes in the behavior of specific individuals to control for individual differences.
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This experiment was carried out to investigate the long-term effects of enhancing cage complexity on behavioural measures of welfare in laboratory rats. We housed 72 rats in groups of four in either 'enriched' or 'unenriched' cages for six weeks. Scan and focal animal sampling were conducted in both the light and dark phase of the second, fourth and sixth weeks. Results revealed that rats in the 'enriched' cages showed longer durations of sleep behaviour, and low levels of agonistic behaviour compared to rats in the 'unenriched' cages. Results importantly demonstrated that the behavioural changes observed in the enriched environment were due to the presence of the enrichments themselves in the cages (indirect effects) and not due merely to rats interacting with the enrichment items in their environment. Thus, enhancing the complexity of conventional laboratory cages can promote behaviour such as longer bouts of sleep that is likely to be indicative of good welfare, and diminish levels of behaviour such as aggression that is likely to lead to poor welfare.
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The assessment of animal welfare relates to investigations of how animals try to cope with their environment, and how easy or how difficult it is for them to do so. The use of rigorous scientific methods to assess this has grown over the past few decades, and so our understanding of the needs of animals has improved during this time. Much of the work in the field of animal welfare has been conducted on farm animals, but it is important to consider how the methods and approaches used in assessing farm animal welfare have been, and can be, adapted and applied to the measurement of welfare in animals in other domains, such as in zoos. This is beneficial to our understanding of both the theoretical knowledge, and the practicability of methods. In this article, some of the commonly-used methods for measuring animal welfare will be discussed, as well as some practical considerations in assessing the welfare of zoo animals.
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In this chapter, sex will refer to the central process of meiosis and syngamy in eukaryotic organisms. Although some form of sexuality characterizes the life cycle of many eukaryotic organisms (i.e., virtually all fungi, plants, and animals), not all eukaryotes are sexual (e.g., many protists) (Margulis 1970, 1996; Bell 1982). Certain asexual protists, for example, only undergo mitosis and never alternate between haploid and diploid stages by way of meiosis and syngamy. Consequently, one of the most fundamental questions in biology is: Why do certain organisms go through meiosis and syngamy while others do not? Despite the apparent simplicity of this query, evolutionary biologists have not provided an entirely satisfactory explanation for the evolution of sex. Much of the difficulty arises because there appears to be no single answer. Moreover, sex is often confused with other associated phenomenon. For instance, one completely subordinate, but intimately related, occurrence is the evolution of gender in organisms that go through meiosis and syngamy. In his essay on the evolution of sex, Ghiselin (1988) aptly wrote, “Gender means the differentiation into males, females, and such alternatives as hermaphrodites. It also includes the differences between sperm and eggs. Such differences are important because they create the circumstances that make sex a puzzle” (p. 9). Yet he dismisses this subject in the next sentence: “Otherwise we are not much concerned about gender either.” Here we clarify the relationship between the evolution of sex and the evolution of gender. This is a critical concept to comprehend because gender differences are nearly universal in sexual organisms. We also discuss some of the major hypotheses proposed to explain why sex exists and recent empirical work that sheds light on the factors that may favor meiosis and syngamy, regardless of gender differences. In the remainder of the chapter, we present a more thorough analysis of the evolution of gender, including a discussion of what the fundamental gender difference is and why there are so many different mechanisms that produce more derived gender differences.
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Brown bears (Ursus arctos) in zoos are often kept under sub-optimal conditions and have behavioral time-budgets that differ from their wild counterparts. We conducted 2 experiments using novel feeding conditions for captive European brown bears (scattering food rather than piling and increasing feeding frequencies from 3 to 6/day) in the Bear Forest (BF), a 2-ha forested enclosure in Rhenen, the Netherlands. No significant differences in any behavioral category were found when food was scattered rather than piled. We found significant differences in active and foraging behavioral categories when feeding was increased form 3 to 6 times daily, suggesting a more natural behavioral pattern. We speculate that this effect will increase when scattering food and increasing feeding frequency are combined into a new feeding condition.
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It is widely acknowledged that environmental enrichment plays an important role in promoting the welfare of captive animals. However, a topic of debate is whether an animal's preference for an enrichment strategy is any indicator of its efficacy. In addition, relatively few studies have evaluated environmental enrichment strategies for non-mammalian species. In the present study, we compared the results of an observational evaluation of enrichment efficacy with the results of a paired-stimulus preference assessment for three Galapagos tortoises. In the observational study, object enrichment (boomer balls and a free-flowing sprinkler) and keeper interactions (shell scrubbing and neck rubbing) were evaluated systematically for their effects on locomotion, species-typical behavior, aggressive and non-aggressive conspecific interactions, and enclosure. Preference assessments were subsequently conducted in which subjects could choose the enrichment strategy to be implemented. All subjects preferred keeper interactions consistently over object enrichment. Our results suggest that enrichment preference was a variable predictor of efficacy across enrichment species-typical behavior, activity levels, enclosure use, and aggressive and non-aggressive conspecific interactions strategies. Preference predicted efficacy for promoting species-typical behavior (1/3 subjects), activity levels (2/3 subjects), and enclosure use (2/3 subjects), but not conspecific interactions (0/3 subjects). The results suggest that preference may be an efficient predictor of enrichment efficacy when daily observational evaluations are not practical; however, the predictive utility of preference assessments may depend on the behavioral goal of the enrichment strategy. We discuss the need for future research examining the relationship between preference and enrichment efficacy-as well as other potential indicators of enrichment effectiveness-in captive animals. (C) 2014 Wiley Periodicals, Inc.
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The value of olfactory enrichment for captive-housed animals is now well recognised. Large cats have been shown to benefit from the introduction of odours to their captive environment, but to date the effect of odour introduction on the behaviour of small cats remains unknown. This study investigated the behaviour of six zoo-housed black-footed cats, Felis nigripes, in response to four odours (no odour [control], nutmeg, catnip and body odour of prey) introduced individually on cloths into the animals’ pens over a period of 5 days. It was hypothesised that the cats’ behaviour would differ significantly between the control and experimental odours and that interest in the experimental odours would wane over time. All of the experimental odours influenced the cats’ behaviour, resulting in an increase in the amount of time that the animals spent in active behaviours, i.e. moving (average increase of 8.3%), grooming (average increase of 5.9%), exploring the cloth (average increase of 10.9%) and exploring the pen (average increase of 9.2%). The experimental odours also resulted in a decrease in the amount of time that the cats spent in sedentary behaviours, i.e. standing (average decrease of 2.8%), sitting (average decrease of 5.2%) and resting (average decrease of 25.9%). Nutmeg exerted less of an effect on the cats’ behaviour than catnip or odour of prey. The cats’ response to all of the experimental odours waned over the course of the 5-day observation period, suggesting that the animals habituated to the stimuli. The results highlight the potential for odour to be employed as a method of environmental enrichment for small captive-housed felids, if presented in an appropriate manner.
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Environmental enrichment programs provide benefits to both captive animals and the facilities that house them, but cost time and resources to design, implement, and maintain. As yet, there have been few theoretically based guidelines to assist animal care staff in establishing cost-efficient enrichment methods that both elicit the desired behavioral changes and maintain their success over time. We describe several well-studied principles from the field of experimental analysis of behavior, including intrinsic reinforcement, extrinsic reinforcement, habituation, extinction, and schedules of reinforcement that could be very useful for evaluating the short- and long-term effectiveness of enrichment. We use this theoretical framework to generate testable hypotheses and provide examples of enrichment studies relevant to our predictions. In particular, we suggest that enrichment devices that offer extrinsic reinforcement (food, social access, etc. as a result of performing behaviors) should produce greater and more prolonged changes in behavior than devices that rely on the behavior itself being reinforcing to the animal. For techniques that provide no extrinsic reinforcement, using stimuli that are novel, are more different from the environment, have been withheld or altered in some way, or are presented less frequently may help reduce habituation. For techniques that provide extrinsic reinforcement, making reinforcement more difficult to obtain and providing more or higher quality reinforcers may increase the long-term success of the enrichment program. In addition, enrichment may be more effective if animal care staff avoid continuously reinforcing behaviors after they are established, enriching immediately after feeding, and exposing animals to enrichment when reinforcement is no longer available. While the current enrichment literature supports the application of behavior analytic theory, empirical evaluation of many of our predictions is still needed.
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This paper summarises recent findings on the causation of stereotypic behaviours and other abnormal repetitive behaviours (ARBs) in captive animals: primarily motivational frustration and/or brain dysfunction, with possible contributory roles also being played by habit-formation and ‘coping’ effects. We then review the extent to which ARBs occur in zoos and similar, estimating that at least 10000 captive wild animals are affected worldwide. We argue for ‘zero tolerance’ of such ARBs, because stress and poor welfare raise ethical issues, while abnormal behavioural phenotypes and possibilities of impaired brain development challenge both the indirect (e.g. educational) and the direct, intrinsic conservation value of affected animals. We then consider five potential means by which ARBs may be tackled: genetic selection; pharmacological treatment; the reinforcement of alternative behaviours; punishment; and environmental enrichment. All except punishment have potentially useful roles to play, but enrichment is the preferred approach: it is most likely to tackle the problems underlying stereotypic behaviours, and thence to improve both welfare and behaviour with few unwanted side-effects. Nevertheless, in zoos, environmental enrichment to date has only had partial success, with no study managing to abolish ARBs in all its subjects—suggesting either that the enrichments currently being used are never quite optimal, or that by the time they are tackled, ARBs have become resistant to change. We suggest some ways in which the effectiveness of enrichments may be enhanced; propose that certain properties of ARBs may usefully help evaluate their likely ‘treatability’; and emphasise that if improving welfare is more important than just reducing ARB, then additional measures are needed in order to first, reliably identify those individuals most at risk from poor welfare, and then, to fully evaluate the welfare impact of enrichments. This paper also emphasises, with examples, the enormous potential value of zoo-derived data for helping understand how taxon, ecological niche, rearing history, and current housing together affect animals’ responses to captivity.
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Captive small felids frequently pace repetitively and/or spend large amounts of time inactive. Presenting a fishing cat with live-fish resulted in more activity (60% less sleeping), increased behavioral diversity, including previously unobserved hunting behaviors, and greater enclosure utilization. Effects persisted for at least 48 h after presentation of live fish, and up to 8 days. In a second study, four leopard cats were fed: (1) once per day, (2) four times per day and, (3) four times per day with food hidden in small piles of brush. Multiple feedings of hidden food increased daily exploratory behavior from 5.5% to over 14%, and increased the diversity of behaviors observed. It also reduced the total duration, and bout length of stereotyped pacing. These studies suggest that providing food to small cats in a way that minimizes predictability of food availability, while maximizing the functional consequences of foraging behavior, can be an effective enrichment technique. These results are discussed in relation to two models of behavioral motivation, one that focuses on the issue of behavioral needs, and the other that emphasizes the importance of information acquisition. © 1993 Wiley-Liss, Inc
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Bell System Technical Journal, also pp. 623-656 (October)
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The physiological and behavioural impact of, as well as preference for, enriched versus barren environments was determined for captive eastern box turtles (Terrapene carolina carolina). Thirty-eight box turtles were randomized to either barren (flat newspaper substrate) or enriched (cypress mulch substrate, shredded paper and a hide box) enclosures for a 1-month period. Complete blood counts, fecal corticosterone, and body weights were measured at the beginning and end of the test period. Activities performed within the two environments were also compared.Turtles in enriched enclosures had a significantly lower heterophil to lymphocyte ratio (H/L) at the end of the treatment period (p=0.01). Enriched-housed turtles also spent significantly less time engaged in escape behaviour (p
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Institutional and federal ethics committees regulate research on live vertebrate animals. Current regulations require researchers to provide environmental enrichment for laboratory animals. The intention is that such enrichment reduces stress and prevents atypical behavior of captive animals, enhancing the ethical treatment of these individuals, as well as providing more robust scientific results. Enrichment can take various forms but most frequently mimics aspects of the animal's natural environment, such as the inclusion of plant life, shelters, conspecifics, or providing challenges to keep the animals occupied. These approaches have proven effective for mammals and birds; however, we know little about the effectiveness of environmental enrichment for other common research taxa, such as reptiles and amphibians. These taxa are more phylogenetically distant from humans, making intuition an unreliable guide upon which to base decisions about ethics best practice, including the benefits of environmental enrichment. The eastern fence lizard, Sceloporus undulatus, spends much of its time off the ground. Therefore, we provided climbing enrichment to captive fence lizards to allow them the opportunity to carry out this common natural behavior in captivity, and tested its effect on a range of ecologic- and scientifically relevant physiological and behavioral parameters. The provision of environmental enrichment, in the form of raised basking platforms, did not affect survival (P=. 0.25), baseline levels of plasma corticosterone (an indicator of physiological stress; P=. 0.81), activity (P=. 0.19), basking behavior (P=. 0.89), time spent hiding (P=. 0.59), growth (mass: P=. 0.44; snout-vent length: P=. 0.47), or overall body condition of these lizards (P=. 0.61). This lack of an effect highlights the need for researchers to objectively test the effectiveness of enrichment, rather than relying on subjectivity and anthropomorphism when making decisions about their use.
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In animal care, when current decisions are made to maximise long-term quality of life (QoL), a key necessity is being able to make accurate predictions about how current choices will affect the animal's future QoL. However, in the procession of any individual's life, many factors that influence QoL change — some are foreseeable, many are not. Moreover, QoL has no fixed anchor points; it is dynamic, mutable, with a shifting frame of reference over time. In addition to actual changes in QoL over time, numerous factors have been identified that influence one's ability to adopt the mindset of the individual at a later point in time — for one's self as well as that of others. It has been shown that in people, across a wide range of health conditions, individuals with illness or disability typically report greater happiness and QoL than do healthy people envisioning themselves in similar circumstances ('the disability paradox'). Difficulties in QoL outcome prediction fall into two categories: (1) predictions made with the wrong mindset, in which there is a mismatch between the mindset of the assessor/predictor and that of the assessee/experiencer; and (2) predictions made on the basis of unforeseen or incorrectly estimated psychological changes in the assessee/experiencer.